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Current surgical management of metastases in the neck from mucosal squamous cell carcinoma of the head and neck
YBJOM-4565; No. of Pages 6
ARTICLE IN PRESS Available online at www.sciencedirect.com
British Journal of Oral and Maxillofacial Surgery xxx (2015) xxx–xxx
Review
Current surgical management of metastases in the neck from mucosal squamous cell carcinoma of the head and neck Ben Green a,∗ , Brian Bisase b , Daryl Godden c , David A. Mitchell d , Peter A. Brennan e a
Craniofacial Unit, Great Ormond Street Hospital for Children, London, UK Department of Oral & Maxillofacial Surgery, Queen Victoria Hospital, East Grinstead, UK c Department of Oral & Maxillofacial Surgery, Gloucestershire Royal Hospital, UK d Maxillofacial Unit, St Luke’s Hospital, Bradford, UK e Department of Oral & Maxillofacial Surgery, Queen Alexandra Hospital, Portsmouth, UK b
Accepted 30 June 2015
Abstract Neck dissection, which is an important method of treatment for metastases from mucosal (and other) squamous cell carcinomas (SCC) of the head and neck, is also useful for staging disease. Since its inception it has changed from a radical to a more conservative procedure, and vital structures are preserved wherever possible. Refinements in methods of imaging to assess involvement in the neck have encouraged alternative approaches that can improve outcomes and reduce morbidity. We look at the reported evidence for the surgical management of metastases in the neck from mucosal SCC. © 2015 Published by Elsevier Ltd. on behalf of The British Association of Oral and Maxillofacial Surgeons.
Keywords: Head and neck squamous cell carcinoma; Neck dissection; Neck metastases; Clinically positive neck; Clinically negative neck; Sentinel lymph node biopsy
Introduction It is well known that evidence of metastases in the neck is an important prognostic factor in patients with mucosal squamous cell carcinomas (SCC) of the head and neck. They can reduce survival by 50%, and regional failure can arise when their treatment is inadequate.1 There is a long-standing principle that the characteristics of the primary tumour (including site and various pathological prognostic indicators) should be used to guide treatment of the neck, but this may not always be the case. Radical neck dissection, which was first introduced ∗ Corresponding author at: Craniofacial Unit, Great Ormond Street Hospital for Children, London, WC1N 3JH. E-mail addresses: [email protected], [email protected] (B. Green), [email protected] (B. Bisase), [email protected] (D. Godden), [email protected] (D.A. Mitchell), [email protected] (P.A. Brennan).
in the late 19th century and for many years was the main treatment for metastases in the neck,2 was modified in the 1950s with preservation of non-lymphatic structures such as the internal jugular vein, muscles, and the nerves associated with function. In the 1980s, selective neck dissection (SND), in which non-lymphatic structures were preserved and only the cervical lymph nodes most likely to contain metastases were removed, was established.3 However, despite its more conservative approach, SND is associated with a degree of morbidity, in particular shoulder dysfunction, and more recently, super-selective neck dissection (SSND), which is limited to 2 levels, has been advocated, and an increasing body of evidence suggests that it is more favourable if used in the proper setting.4 The current classification and terminology for neck dissection was introduced in 1991 by a committee of the American Head and Neck Society and the American Academy of Otolaryngology - Head and Neck Surgery. The terminology was
http://dx.doi.org/10.1016/j.bjoms.2015.06.025 0266-4356/© 2015 Published by Elsevier Ltd. on behalf of The British Association of Oral and Maxillofacial Surgeons.
Please cite this article in press as: Green B, et al. Current surgical management of metastases in the neck from mucosal squamous cell carcinoma of the head and neck. Br J Oral Maxillofac Surg (2015), http://dx.doi.org/10.1016/j.bjoms.2015.06.025
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Table 1 Classifications of neck dissection. 2002 classification5 (American Head and Neck Society and Committee for Head and Neck Surgery and Oncology; American Academy of Otolaryngology- Head and Neck Surgery) Radical neck dissection
Modified radical neck dissection Selective neck dissection Extended neck dissection
2008 classification6 (American Head and Neck Society and Committee for Head and Neck Surgery and Oncology; American Academy of Otolaryngology- Head and Neck Surgery) Classification and terminology did not change but new recommendations were made regarding boundaries between levels I and II and levels III, IV and VI; terminology of the superior mediastinal nodes (level VII); and method of submitting specimens for analysis No change No change No change
updated in 2002 and 2008 (Table 1),5,6 and in the last update, lymph nodes in the neck were grouped in levels. Recently, Ferlito et al proposed a new classification for neck dissection in which all types are classified as ND. The non-lymphatic structures and levels are indicated in parentheses unlike the other methods in which the non-lymphatic structures are not recorded.7 SCC of the oral cavity in patients with no sign of metastases in the neck (N0) Occult metastases have been reported in between 20% and 44% of patients with SCC of the oral cavity and no sign of metastases in the neck.8–10 It is generally agreed that elective neck dissection is indicated in those with clinically N0 oral SCC when the risk of occult metastases exceeds 15% - 20%, but in most cases it may not be necessary. Observation, which reserves neck dissection for salvage of regional recurrence, is one alternative,11 but the quality of the initial and follow-up examination of the neck, and the postoperative assessment are vitally important. This study compared observation (n=234) with neck dissection (n=51) in 285 patients with clinically N0 necks after initial investigation with ultrasound-guided fine needle aspiration cytology (FNAC) to detect occult metastases. In the observation group 27.8% developed metastases, and most required radical neck dissection and adjuvant radiotherapy. However, 5-year disease-specific and overall survival rates were almost the same as those for elective neck dissection. Although elective neck dissection may cause less morbidity than radical neck dissection, most patients with clinically N0 necks do not have occult metastases. Therefore, the need to identify those who do and who could be offered less radical, early, elective treatment is clear.11 It is also important to recognise that although ultrasound-guided FNAC has high diagnostic sensitivity and specificity, some surgeons now also do sentinel lymph node biopsy (SLNB). A common prognostic indicator of an increased risk of occult metastases is the thickness of the primary tumour. Leusink et al found that occult lymph node metastases were
2011 classification proposed by Ferlito et al7
Any neck dissection is designated ND. Level from which lymph nodes are removed, or the sublevels or non-lymphatic structures, or both, are shown in parentheses
No change No change No change
more likely when the tumour was more than 4 mm thick.12 However, tumours with different thicknesses can result in occult metastases, and other factors such as vascular and perineural invasion are also implicated. A radical or modified radical neck dissection is not necessary in patients with clinically N0 necks, as comparable results have been obtained with SND (with adjuvant radiotherapy if indicated histopathologically). Levels I, IIa, and III are at highest risk for metastases, so they should be included in the dissection. While metastases to level IIb are rare in tumours anterior to the first molar teeth, nodes at this level may be involved in 22% of patients who have metastatic disease in the level IIa nodes.12 Surgeons should therefore consider whether to include this level in the neck dissection and in planned postoperative radiotherapy. It is not clear whether level IV should be included in patients with clinically N0 necks because although the incidence of metastases is low in this level, a proportion seem to skip to levels III and IV.13 However, in patients with SCC of the tongue it is important to appreciate that in some cases level IV is not the only site in the neck that is affected. It is likely that the level IV skip metastases found in the original study by Woolgar et al actually arose in level III, and there is now good evidence to avoid level IV in patients with cN0 oral SCC.14 There is general consensus that level V is rarely involved.15 In a retrospective analysis of 35 patients with tumours at various stages, Godden at al compared elective neck dissection (n = 18) with observation (n = 17).16 The time taken for recurrence to develop was the same in both groups. In 27 patients, the primary tumour was more than 5 mm thick. Recurrence, particularly at level II confirms that meticulous dissection is needed in this area and that tumour thickness must be considered when planning the treatment of patients with clinically N0 necks.16 Laryngeal SCC in patients with N0 necks As a result of their different embryological origins, the supraglottic, glottic, and subglottic components drain through
Please cite this article in press as: Green B, et al. Current surgical management of metastases in the neck from mucosal squamous cell carcinoma of the head and neck. Br J Oral Maxillofac Surg (2015), http://dx.doi.org/10.1016/j.bjoms.2015.06.025
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different routes. Metastases from the supraglottic larynx can occur even in the early stages of cancer, but metastases from early glottic cancers are rare.17 They usually occur in levels II, III, and IV, but levels I and V are rarely involved, so SND of levels II-IV (anterolateral neck dissection) has been widely and successfully used in the management of the clinically N0 neck, with recurrence of only 1.7%.18 Despite the spinal accessory nerve (SAN) being spared during SND of levels II-IV, its function can be impaired after operation because of neurapraxia during clearance of level IIb, or devascularisation during dissection.19,20 In prospective studies, the rate of metastases in level IIb in patients with clinically N0 necks ranges from 0 - 3.2%,21,22 so dissection of this level is not usually indicated, which minimises dysfunction of the nerve. However, if level IIa nodes are involved then level IIb should be considered for inclusion in the neck dissection or in postoperative radiotherapy. There is also a low rate of metastases to level IV, so it is possible to leave this level to minimise other potential complications such as injury to the phrenic nerve and damage to the thoracic duct. Based on this, patients with supraglottic SCC can have neck dissection that removes levels II and III. This super-selective neck dissection (SSND) is defined as the removal of up to 2 contiguous levels.23 However, it has recently been reported that level VI metastases are often found in patients with subglottic, advanced glottic, and some advanced supraglottic SCC, therefore, in these cases it should be included in the dissection.24 Oropharyngeal and hypopharyngeal SCC in patients with N0 necks The management of the clinically N0 neck in these patients is less clear. The risk of occult metastases in patients with oropharyngeal SCC is high with an incidence of 39% in those with a clinically N0 neck,25 which suggests that neck dissection is necessary. However, the efficacy of treatment in these patients has not been shown in prospective studies. It has been reported that in 49 patients, 10% in the neck dissection group, and 24% in the observation group had neck recurrence, but salvage was successful in only half of those with recurrences in the observation group.26 Oropharyngeal SCC primarily drains to levels II- IV and to the parapharyngeal and retropharyngeal lymph nodes,27,28 so dissection of the lymph nodes at these levels seems to be appropriate in patients with oropharyngeal SCC and a clinically N0 neck. It has been shown that most metastases are found in levels II and III. Those in level IIb have been identified in only 2.5% - 6% of patients with oropharyngeal SCC, so it is questionable whether this level needs to be included in the dissection when there are no signs of metastases in the neck. In their study of 348 patients, Gross et al found metastases at level IIb in 25% of patients with, and 2.5% of patients without metastic disease in the neck,25 and concluded that level IV metastases are rare in patients with clinically N0 necks. Transoral, or video and robotic-assisted resection is increasingly being used to treat oropharyngeal SCC. The
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incidence of bilateral lymph node metastases was 15% in T1 tumours of the base of the tongue and T1 and T2 tumours of the tonsillar fossa, which raises questions about whether a unilateral or bilateral neck dissection is required in these cases.29 Drainage from the hypopharynx is different. The pyriform sinus drains into the upper and jugular chains, while the inferior hypopharynx drains into the paratracheal, paraoesophageal, and supraclavicular lymph nodes. Levels II-IV were most often involved with these tumours.30 Sakai et al showed that there were metastases in sublevel IIb in 13.3% of patients with hypopharyngeal tumours who had some metastases in the neck but there were none in those with clinically N0 necks.31 SCC at other sites in the head and neck in patients with N0 necks Currently, in patients with SCC at less commonly affected sites such as the paranasal sinuses and clinically N0 necks, there is a lack of data regarding neck dissection. Takes et al reviewed the management of SCC of the maxillary sinus.32 The studies included were heterogeneous in terms of stage, histopathological findings, and management. The high rates of failure meant that elective neck dissection was seen as an advantage so they recommended elective neck dissection, particularly in patients who needed reconstruction with a free-flap or irradiation of the neck and site of the primary tumour.32 SCC of the head and neck in patients with clinical signs of metastases in the neck (N+) In patients with a clinically invaded neck, a radical or modified radical neck dissection is often considered to be unnecessary as not all the palpable and involved nodes contain metastases, and not all the levels are affected. Kowalski and Carvalho analysed 164 patients with oral SCC who had N1 or N2a necks, and found that a high rate of those with N1 disease had invaded nodes at level I.33 They reported a false positive rate of 32%.33 SND has been studied to find out whether it is effective without compromising oncological safety. Andersen et al explored 129 selective neck dissections in 106 patients with previously treated N1-N3 SCC of the head and neck.34 Regional control was 94.3% and there were 6 recurrences. In another study of 34 selective neck dissections in 28 patients there were 4 recurrences (11.8%). More regional recurrences were found in patients with advanced T stages than in those with early T stage disease.35 Dhiwaker et al found that in most patients, nodal disease was confined to only one or two levels. There was no regional recurrence after primary treatment and after radiotherapy the rate was 13%.36 Careful planning and discussion by the multidisciplinary team are needed for all of these patients, but SND
Please cite this article in press as: Green B, et al. Current surgical management of metastases in the neck from mucosal squamous cell carcinoma of the head and neck. Br J Oral Maxillofac Surg (2015), http://dx.doi.org/10.1016/j.bjoms.2015.06.025
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may be feasible when there are metastases in the neck and no other structures are involved (such as the sternomastoid or internal jugular vein). Adjuvant treatment that has wellrecognised pathological indications may also be required. For SCC at other rarer sites (such as the gingiva), Lubek et al assessed 111 cases of gingival carcinoma to find out whether there were indications for elective neck dissection. Most patients had T3/T4 disease, and 42% of them had nodal involvement.37 The authors concluded that elective neck dissection was indicated for all patients who present with mandibular gingival tumours and T3/T4 gingival carcinomas of the maxilla, as regional metastatic behaviour is more aggressive.38 However, Beltramini et al found that only 21% of the patients studied had cervical nodal involvement but regional metastatic behaviour was more aggressive than at other sites.39 These findings are similar those of Brown et al40 who found recurrence in the maxillary alveolus and hard palate in 26% of cases. The management of SCC of the maxillary sinus remains controversial. Of the 18 patients reviewed in another paper by Brown et al., 13 had elective SND. Four had regional metastases: 2 had nodal disease confirmed after the operation, and 2 who had had no pathological sign of disease in the neck, developed regional recurrence. The authors reported a recurrence rate of 11% compared with 12% in other reports, and they concluded that there was no evidence that elective SND results in better disease control.41 Brown et al also reported that neck dissection is not required for SCC of the maxillary sinus and that postoperative radiotherapy should always be considered. However, when free flap reconstruction is used, the neck is usually accessed for the anastomosis of vessels (although other sites such as the superficial temporal vessels can sometimes be used). In patients who do not have microvascular reconstruction (for example, when obturators or a temporalis flap is used), or neck dissection, it could lead to under-staging of the neck.40 Neck dissection after chemoradiotherapy for mucosal SCC of the head and neck An elective neck dissection may be beneficial for patients with persistent or recurrent resectable disease in the neck after chemoradiotherapy.42 However, the therapeutic effects of chemoradiotherapy continue long after treatment, and the sampling of cervical lymph nodes may produce falsepositive results for many weeks or even months.43 The optimal time for assessing response as identified by computed tomography (CT), magnetic resonance imaging (MRI), or positron emission tomography (PET)-CT, is 8 -12 weeks after chemoradiotherapy.44 It had been thought that delaying the operation for more than 12 weeks reduces disease control in the neck, but the evidence is not entirely clear.45 In a review, Ferlito et al evaluated the necessity of planned neck dissection in patients who responded completely to chemoradiotherapy.46 A total of 24 studies showed that neck dissection gave an advantage, and among them, regional
failures varied from 0 - 38%. However, in 26, elective neck dissection was not advantageous. Most of the studies reported regional failure rates of between 0 and 16%, which are comparable to those of elective neck dissection. PET-CT may help to detect persistent or recurrent disease in the neck, and an elective neck dissection in patients with a complete response to chemoradiotherapy after 12 weeks would be difficult to justify.47,48 Evidence is emerging that, when clinically possible, SND can be done after chemoradiotherapy in most patients.49,50 However, the results included patients with bulky neck disease who had, and had not had, a complete response to chemoradiotherapy. A total of 62 patients had 69 operations (SND), and in most, residual disease was confined to levels II and III. Robbins et al explored the feasibility of SSND after chemoradiotherapy. Initially, the data were based on 177 patients (with clinically involved necks) who had concomitant chemotherapy and radiotherapy, and comparisons were made between those with disease in specific levels when it was restaged after chemotherapy, and the evidence of pathological disease. In those whose necks were restaged as a “partial response”, 73 had evidence of residual lymphadenopathy at one level. A total of 57 patients had salvage neck dissection and 2 had evidence of disease that extended beyond one level. This raises the possibility that SSND can be done if residual nodal disease is confined to a single level.51 In another study, Robbins et al included 241 patients with stage IV SCC of the head and neck who had had SND, SSND, or radical or MRND, and found that SSND was effective in a subgroup of patients after chemoradiotherapy. It could be seen as an adjuvant, as opposed to primary treatment, and is based on the principle that levels with no clinical sign of metastases before treatment had a therapeutic dose of radiation plus chemotherapy, which would obviate the need for them to be removed despite there being signs of disease in other levels. It must be remembered that lymphatic drainage changes unpredictably after surgical or non-surgical oncological treatment of the neck. However, if SND or SSND is done, in 20% of cases the internal jugular vein, sternocleidomastoid, or spinal accessory nerve is removed for adequate resection.52,53 Sentinel lymph node biopsy (SLNB) The use of SLNB has become established for early oral cancer and has been recommended as an alternative to neck dissection in patients with T1-T2 N0 disease.54,55 Gurney et al suggested that it can be used to identify different prognostic groups, which would allow better tailoring of treatment, and enable more focused management of the neck.56 It has also been identified as the most cost-effective procedure in the management of N0 in early oral cancer.57,58 It can accurately detect occult metastases and has good long-term disease control at the site affected in patients who have the procedure alone,59 and also causes less postoperative morbidity than
Please cite this article in press as: Green B, et al. Current surgical management of metastases in the neck from mucosal squamous cell carcinoma of the head and neck. Br J Oral Maxillofac Surg (2015), http://dx.doi.org/10.1016/j.bjoms.2015.06.025
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elective neck dissection. 60 Flach et al found that SLNB reduced the risk of occult metastases from 40% to 8% in patients with T1/T2 oral SCC. 61 When sentinel nodes were not involved, control in the neck was 97%; when they were involved it was 95%. Den Toom et al found that SLNB had a sensitivity of 93%, and advocated its use primarily for T1/T2 oral SCC.62 It can also be used as a safe and accurate method of staging to select patients with clinically stage I/II oropharyngeal SCC and occult lymph node metastases for elective neck dissection,63 and in patients with carcinoma of the floor of the mouth.64 Some advocate its use in patients who have previously had the neck treated. However, the rate of detection varies and depends on whether they had ipsilateral, contralateral, or bilateral neck dissection. Despite this, it can also be useful in the assessment of individual lymphatic drainage patterns.65 Excellent control in the neck, which compares well with elective neck dissection, can be achieved in patients who have not had a neck dissection and have no sign of disease on SLNB.56 Conclusion There seems to be an interest in super selective neck dissection, and with advances in diagnostic imaging (including SLNB and PET-CT) the tailoring of individual treatment plans for the neck is likely to become the next major development. Conflict of Interest We have no conflicts of interest
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30. Candela FC, Kothari K, Shah JP. Patterns of cervical node metastases from squamous carcinoma of the oropharynx and hypopharynx. Head Neck 1990;12:197–203. 31. Sakai A, Okami K, Sugimoto R, et al. Evaluating the significance of level IIb neck dissection for hypopharyngeal cancer. Head Neck 2013;35:1777–80. 32. Takes RP, Ferlito A, Silver CE, et al. The controversy in the management of the N0 neck for squamous cell carcinoma of the maxillary sinus. Eur Arch Otorhinolaryngol 2014;271:899–904. 33. Kowalski LP, Carvalho AL. Feasibility of supraomohyoid neck dissection in N1 and N2a oral cancer patients. Head Neck 2002;24:921–4. 34. Andersen PE, Warren F, Spiro J, et al. Results of selective neck dissection in management of the node-positive neck. Arch Otolaryngol Head Neck Surg 2002;128:1180–4. 35. Santos AB, Cernea CR, Inoue M, et al. Selective neck dissection for nodepositive necks in patients with head and neck squamous cell carcinoma: a word of caution. Arch Otolaryngol Head Neck Surg 2006;132:79–81. 36. Dhiwakar M, Robbins KT, Rao K, et al. Efficacy of selective neck dissection for nodal metastasis with involvement of nonlymphatic structures. Head Neck 2011;33:1099–105. 37. Lubek J, El-Hakim M, Salama AR, et al. Gingival carcinoma: retrospective analysis of 72 patients and indications of neck dissection. Br J Oral Maxillofac Surg 2011;49:182–5. 38. Montes DM, Carlson ER, Fernandes R, et al. Oral maxillary squamous cell carcinoma: an indication for neck dissection in the clinically negative neck. Head Neck 2011;33:1581–5. 39. Beltramini GA, Massarelli O, Demarchi M, et al. Is neck dissection needed in squamous-cell carcinoma of the maxillary gingiva, alveolus, and hard palate? A multicentre Italian study of 65 cases and literature review. Oral Oncol 2012;48:97–101. 40. Brown JS, Bekiroglu F, Shaw RJ, et al. Management of the neck and regional recurrence in squamous cell carcinoma of the maxillary alveolus and hard palate compared with other sites in the oral cavity. Head Neck 2013;35:265–9. 41. Brown JS, Bekiroglu F, Shaw RJ, et al. First report of elective selective neck dissection in the management of squamous cell carcinoma of the maxillary sinus. Br J Oral Maxillofac Surg 2013;51:103–7. 42. Hamoir M, Ferlito A, Schmitz S, et al. The role of neck dissection in the setting of chemoradiation therapy for head and neck squamous cell carcinoma with advanced neck disease. Oral Oncol 2012;48:203–10. 43. Kwong DL, Nicholls J, Wei WI, et al. The time course of histologic remission after treatment of patients with nasopharyngeal carcinoma. Cancer 1999;85:1446–53. 44. Wee JT, Anderson BO, Corry J, et al. Management of the neck after chemoradiotherapy for head and neck cancers in Asia: consensus statement from the Asian Oncology Summit 2009. Lancet Oncol 2009;10:1086–92. 45. Lavertu P, Bonafede JP, Adelstein DJ, et al. Comparison of surgical complications after organ-preservation therapy in patients with stage III or IV squamous cell head and neck cancer. Arch Otolaryngol Head Neck Surg 1998;124:401–6. 46. Ferlito A, Corry J, Silver CE, et al. Planned neck dissection for patients with complete response to chemoradiotherapy: a concept approaching obsolescence. Head Neck 2010;32:253–61. 47. Goguen LA, Chapuy CI, Li Y, et al. Neck dissection after chemoradiotherapy: timing and complications. Arch Otolaryngol Head Neck Surg 2010;136:1071–7.
48. Robbins KT, Wong FS, Kumar P, et al. Efficacy of targeted chemoradiation and planned selective neck dissection to control bulky nodal disease in advanced head and neck cancer. Arch Otolaryngol Head Neck Surg 1999;125:670–5. 49. Hillel AT, Fakhry C, Pai SI, et al. Selective versus comprehensive neck dissection after chemoradiation for advanced oropharyngeal squamous cell carcinoma. Otolaryngol Head Neck Surg 2009;141:737–42. 50. Stenson KM, Haraf DJ, Pelzer H, et al. The role of cervical lymphadenectomy after aggressive comcomitant chemoradiotherapy: the feasibility of selective neck dissection. Arch Otolaryngol Head Neck Surg 2000;126:950–6. 51. Robbins KT, Shannon K, Vieira F. Superselective neck dissection after chemoradiation: feasibility based on clinical and pathologic comparisons. Arch Otolaryngol Head Neck Surg 2007;133:486–9. 52. Robbins KT, Dhiwakar M, Vieira F, et al. Efficacy of super-selective neck dissection following chemoradiation for advanced head and neck cancer. Oral Oncol 2012;48:1185–9. 53. Cannady SB, Lee WT, Scharpf J, et al. Extent of neck dissection required after concurrent chemoradiation for stage IV head and neck squamous cell carcinoma. Head Neck 2010;32:348–56. 54. Broglie MA, Haile SR, Stoeckli SJ. Long-term experience in sentinel lymph node biopsy for early oral and oropharyngeal squamous cell carcinoma. Ann Surg Oncol 2011;18:2732–8. 55. Civantos FJ, Stoeckli SJ, Takes RP, et al. What is the role of sentinel lymph node biopsy in the management of oral cancer in 2010? Eur Arch Otorhinolaryngol 2010;267:839–44. 56. Gurney BA, Schilling C, Putcha V, et al. Implications of a positive sentinel node in oral squamous cell carcinoma. Head Neck 2012;34:1580–5. 57. Govers TM, Hannink G, Merkx MA, et al. Sentinel node biopsy for squamous cell carcinoma of the oral cavity and oropharynx: a diagnostic meta-analysis. Oral Oncol 2013;49:726–32. 58. O’Connor R, Pezier T, Schilling C, et al. The relative cost of sentinel lymph node biopsy in early oral cancer. J Craniomaxillofac Surg 2013;41:721–7. 59. Pezier T, Nixon IJ, Gurney B, et al. Sentinel lymph node biopsy for T1/T2 oral cavity squamous cell carcinoma-a prospective case series. Ann Surg Oncol 2012;19:3528–33. 60. Murer K, Huber GF, Haile SR, et al. Comparison of morbidity between sentinel node biopsy and elective neck dissection for treatment of the N0 neck in patients with oral squamous cell carcinoma. Head Neck 2011;33:1260–4. 61. Flach GB, Bloemena E, Klop WM, et al. Sentinel lymph node biopsy in clinically N0 T1-T2 staged oral cancer: the Dutch multicenter trial. Oral Oncol 2014;50:1020–4. 62. Den Toom IJ, Heuveling DA, Flach GB, et al. Sentinel node biopsy for early-stage oral cavity cancer: the VU University Medical Center experience. Head Neck 2015;37:573–8. 63. Broglie MA, Haerle SK, Huber GF, et al. Occult metastases detected by sentinel node biopsy in patients with early oral and oropharyngeal squamous cell carcinoma: impact on survival. Head Neck 2013;35:660–6. 64. Alvarez J, Bidaguren A, McGurk M, et al. Sentinel node biopsy in relation to survival in floor of the mouth carcinoma. Int J Oral Maxillofac Surg 2014;43:269–73. 65. Flach GB, Broglie MA, van Schie A, et al. Sentinel node biopsy for oral and oropharyngeal squamous cell carcinoma in the previously treated neck. Oral Oncol 2012;48:85–9.
Please cite this article in press as: Green B, et al. Current surgical management of metastases in the neck from mucosal squamous cell carcinoma of the head and neck. Br J Oral Maxillofac Surg (2015), http://dx.doi.org/10.1016/j.bjoms.2015.06.025
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Review
Current surgical management of metastases in the neck from mucosal squamous cell carcinoma of the head and neck Ben Green a,∗ , Brian Bisase b , Daryl Godden c , David A. Mitchell d , Peter A. Brennan e a
Craniofacial Unit, Great Ormond Street Hospital for Children, London, UK Department of Oral & Maxillofacial Surgery, Queen Victoria Hospital, East Grinstead, UK c Department of Oral & Maxillofacial Surgery, Gloucestershire Royal Hospital, UK d Maxillofacial Unit, St Luke’s Hospital, Bradford, UK e Department of Oral & Maxillofacial Surgery, Queen Alexandra Hospital, Portsmouth, UK b
Accepted 30 June 2015
Abstract Neck dissection, which is an important method of treatment for metastases from mucosal (and other) squamous cell carcinomas (SCC) of the head and neck, is also useful for staging disease. Since its inception it has changed from a radical to a more conservative procedure, and vital structures are preserved wherever possible. Refinements in methods of imaging to assess involvement in the neck have encouraged alternative approaches that can improve outcomes and reduce morbidity. We look at the reported evidence for the surgical management of metastases in the neck from mucosal SCC. © 2015 Published by Elsevier Ltd. on behalf of The British Association of Oral and Maxillofacial Surgeons.
Keywords: Head and neck squamous cell carcinoma; Neck dissection; Neck metastases; Clinically positive neck; Clinically negative neck; Sentinel lymph node biopsy
Introduction It is well known that evidence of metastases in the neck is an important prognostic factor in patients with mucosal squamous cell carcinomas (SCC) of the head and neck. They can reduce survival by 50%, and regional failure can arise when their treatment is inadequate.1 There is a long-standing principle that the characteristics of the primary tumour (including site and various pathological prognostic indicators) should be used to guide treatment of the neck, but this may not always be the case. Radical neck dissection, which was first introduced ∗ Corresponding author at: Craniofacial Unit, Great Ormond Street Hospital for Children, London, WC1N 3JH. E-mail addresses: [email protected], [email protected] (B. Green), [email protected] (B. Bisase), [email protected] (D. Godden), [email protected] (D.A. Mitchell), [email protected] (P.A. Brennan).
in the late 19th century and for many years was the main treatment for metastases in the neck,2 was modified in the 1950s with preservation of non-lymphatic structures such as the internal jugular vein, muscles, and the nerves associated with function. In the 1980s, selective neck dissection (SND), in which non-lymphatic structures were preserved and only the cervical lymph nodes most likely to contain metastases were removed, was established.3 However, despite its more conservative approach, SND is associated with a degree of morbidity, in particular shoulder dysfunction, and more recently, super-selective neck dissection (SSND), which is limited to 2 levels, has been advocated, and an increasing body of evidence suggests that it is more favourable if used in the proper setting.4 The current classification and terminology for neck dissection was introduced in 1991 by a committee of the American Head and Neck Society and the American Academy of Otolaryngology - Head and Neck Surgery. The terminology was
http://dx.doi.org/10.1016/j.bjoms.2015.06.025 0266-4356/© 2015 Published by Elsevier Ltd. on behalf of The British Association of Oral and Maxillofacial Surgeons.
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Table 1 Classifications of neck dissection. 2002 classification5 (American Head and Neck Society and Committee for Head and Neck Surgery and Oncology; American Academy of Otolaryngology- Head and Neck Surgery) Radical neck dissection
Modified radical neck dissection Selective neck dissection Extended neck dissection
2008 classification6 (American Head and Neck Society and Committee for Head and Neck Surgery and Oncology; American Academy of Otolaryngology- Head and Neck Surgery) Classification and terminology did not change but new recommendations were made regarding boundaries between levels I and II and levels III, IV and VI; terminology of the superior mediastinal nodes (level VII); and method of submitting specimens for analysis No change No change No change
updated in 2002 and 2008 (Table 1),5,6 and in the last update, lymph nodes in the neck were grouped in levels. Recently, Ferlito et al proposed a new classification for neck dissection in which all types are classified as ND. The non-lymphatic structures and levels are indicated in parentheses unlike the other methods in which the non-lymphatic structures are not recorded.7 SCC of the oral cavity in patients with no sign of metastases in the neck (N0) Occult metastases have been reported in between 20% and 44% of patients with SCC of the oral cavity and no sign of metastases in the neck.8–10 It is generally agreed that elective neck dissection is indicated in those with clinically N0 oral SCC when the risk of occult metastases exceeds 15% - 20%, but in most cases it may not be necessary. Observation, which reserves neck dissection for salvage of regional recurrence, is one alternative,11 but the quality of the initial and follow-up examination of the neck, and the postoperative assessment are vitally important. This study compared observation (n=234) with neck dissection (n=51) in 285 patients with clinically N0 necks after initial investigation with ultrasound-guided fine needle aspiration cytology (FNAC) to detect occult metastases. In the observation group 27.8% developed metastases, and most required radical neck dissection and adjuvant radiotherapy. However, 5-year disease-specific and overall survival rates were almost the same as those for elective neck dissection. Although elective neck dissection may cause less morbidity than radical neck dissection, most patients with clinically N0 necks do not have occult metastases. Therefore, the need to identify those who do and who could be offered less radical, early, elective treatment is clear.11 It is also important to recognise that although ultrasound-guided FNAC has high diagnostic sensitivity and specificity, some surgeons now also do sentinel lymph node biopsy (SLNB). A common prognostic indicator of an increased risk of occult metastases is the thickness of the primary tumour. Leusink et al found that occult lymph node metastases were
2011 classification proposed by Ferlito et al7
Any neck dissection is designated ND. Level from which lymph nodes are removed, or the sublevels or non-lymphatic structures, or both, are shown in parentheses
No change No change No change
more likely when the tumour was more than 4 mm thick.12 However, tumours with different thicknesses can result in occult metastases, and other factors such as vascular and perineural invasion are also implicated. A radical or modified radical neck dissection is not necessary in patients with clinically N0 necks, as comparable results have been obtained with SND (with adjuvant radiotherapy if indicated histopathologically). Levels I, IIa, and III are at highest risk for metastases, so they should be included in the dissection. While metastases to level IIb are rare in tumours anterior to the first molar teeth, nodes at this level may be involved in 22% of patients who have metastatic disease in the level IIa nodes.12 Surgeons should therefore consider whether to include this level in the neck dissection and in planned postoperative radiotherapy. It is not clear whether level IV should be included in patients with clinically N0 necks because although the incidence of metastases is low in this level, a proportion seem to skip to levels III and IV.13 However, in patients with SCC of the tongue it is important to appreciate that in some cases level IV is not the only site in the neck that is affected. It is likely that the level IV skip metastases found in the original study by Woolgar et al actually arose in level III, and there is now good evidence to avoid level IV in patients with cN0 oral SCC.14 There is general consensus that level V is rarely involved.15 In a retrospective analysis of 35 patients with tumours at various stages, Godden at al compared elective neck dissection (n = 18) with observation (n = 17).16 The time taken for recurrence to develop was the same in both groups. In 27 patients, the primary tumour was more than 5 mm thick. Recurrence, particularly at level II confirms that meticulous dissection is needed in this area and that tumour thickness must be considered when planning the treatment of patients with clinically N0 necks.16 Laryngeal SCC in patients with N0 necks As a result of their different embryological origins, the supraglottic, glottic, and subglottic components drain through
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different routes. Metastases from the supraglottic larynx can occur even in the early stages of cancer, but metastases from early glottic cancers are rare.17 They usually occur in levels II, III, and IV, but levels I and V are rarely involved, so SND of levels II-IV (anterolateral neck dissection) has been widely and successfully used in the management of the clinically N0 neck, with recurrence of only 1.7%.18 Despite the spinal accessory nerve (SAN) being spared during SND of levels II-IV, its function can be impaired after operation because of neurapraxia during clearance of level IIb, or devascularisation during dissection.19,20 In prospective studies, the rate of metastases in level IIb in patients with clinically N0 necks ranges from 0 - 3.2%,21,22 so dissection of this level is not usually indicated, which minimises dysfunction of the nerve. However, if level IIa nodes are involved then level IIb should be considered for inclusion in the neck dissection or in postoperative radiotherapy. There is also a low rate of metastases to level IV, so it is possible to leave this level to minimise other potential complications such as injury to the phrenic nerve and damage to the thoracic duct. Based on this, patients with supraglottic SCC can have neck dissection that removes levels II and III. This super-selective neck dissection (SSND) is defined as the removal of up to 2 contiguous levels.23 However, it has recently been reported that level VI metastases are often found in patients with subglottic, advanced glottic, and some advanced supraglottic SCC, therefore, in these cases it should be included in the dissection.24 Oropharyngeal and hypopharyngeal SCC in patients with N0 necks The management of the clinically N0 neck in these patients is less clear. The risk of occult metastases in patients with oropharyngeal SCC is high with an incidence of 39% in those with a clinically N0 neck,25 which suggests that neck dissection is necessary. However, the efficacy of treatment in these patients has not been shown in prospective studies. It has been reported that in 49 patients, 10% in the neck dissection group, and 24% in the observation group had neck recurrence, but salvage was successful in only half of those with recurrences in the observation group.26 Oropharyngeal SCC primarily drains to levels II- IV and to the parapharyngeal and retropharyngeal lymph nodes,27,28 so dissection of the lymph nodes at these levels seems to be appropriate in patients with oropharyngeal SCC and a clinically N0 neck. It has been shown that most metastases are found in levels II and III. Those in level IIb have been identified in only 2.5% - 6% of patients with oropharyngeal SCC, so it is questionable whether this level needs to be included in the dissection when there are no signs of metastases in the neck. In their study of 348 patients, Gross et al found metastases at level IIb in 25% of patients with, and 2.5% of patients without metastic disease in the neck,25 and concluded that level IV metastases are rare in patients with clinically N0 necks. Transoral, or video and robotic-assisted resection is increasingly being used to treat oropharyngeal SCC. The
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incidence of bilateral lymph node metastases was 15% in T1 tumours of the base of the tongue and T1 and T2 tumours of the tonsillar fossa, which raises questions about whether a unilateral or bilateral neck dissection is required in these cases.29 Drainage from the hypopharynx is different. The pyriform sinus drains into the upper and jugular chains, while the inferior hypopharynx drains into the paratracheal, paraoesophageal, and supraclavicular lymph nodes. Levels II-IV were most often involved with these tumours.30 Sakai et al showed that there were metastases in sublevel IIb in 13.3% of patients with hypopharyngeal tumours who had some metastases in the neck but there were none in those with clinically N0 necks.31 SCC at other sites in the head and neck in patients with N0 necks Currently, in patients with SCC at less commonly affected sites such as the paranasal sinuses and clinically N0 necks, there is a lack of data regarding neck dissection. Takes et al reviewed the management of SCC of the maxillary sinus.32 The studies included were heterogeneous in terms of stage, histopathological findings, and management. The high rates of failure meant that elective neck dissection was seen as an advantage so they recommended elective neck dissection, particularly in patients who needed reconstruction with a free-flap or irradiation of the neck and site of the primary tumour.32 SCC of the head and neck in patients with clinical signs of metastases in the neck (N+) In patients with a clinically invaded neck, a radical or modified radical neck dissection is often considered to be unnecessary as not all the palpable and involved nodes contain metastases, and not all the levels are affected. Kowalski and Carvalho analysed 164 patients with oral SCC who had N1 or N2a necks, and found that a high rate of those with N1 disease had invaded nodes at level I.33 They reported a false positive rate of 32%.33 SND has been studied to find out whether it is effective without compromising oncological safety. Andersen et al explored 129 selective neck dissections in 106 patients with previously treated N1-N3 SCC of the head and neck.34 Regional control was 94.3% and there were 6 recurrences. In another study of 34 selective neck dissections in 28 patients there were 4 recurrences (11.8%). More regional recurrences were found in patients with advanced T stages than in those with early T stage disease.35 Dhiwaker et al found that in most patients, nodal disease was confined to only one or two levels. There was no regional recurrence after primary treatment and after radiotherapy the rate was 13%.36 Careful planning and discussion by the multidisciplinary team are needed for all of these patients, but SND
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may be feasible when there are metastases in the neck and no other structures are involved (such as the sternomastoid or internal jugular vein). Adjuvant treatment that has wellrecognised pathological indications may also be required. For SCC at other rarer sites (such as the gingiva), Lubek et al assessed 111 cases of gingival carcinoma to find out whether there were indications for elective neck dissection. Most patients had T3/T4 disease, and 42% of them had nodal involvement.37 The authors concluded that elective neck dissection was indicated for all patients who present with mandibular gingival tumours and T3/T4 gingival carcinomas of the maxilla, as regional metastatic behaviour is more aggressive.38 However, Beltramini et al found that only 21% of the patients studied had cervical nodal involvement but regional metastatic behaviour was more aggressive than at other sites.39 These findings are similar those of Brown et al40 who found recurrence in the maxillary alveolus and hard palate in 26% of cases. The management of SCC of the maxillary sinus remains controversial. Of the 18 patients reviewed in another paper by Brown et al., 13 had elective SND. Four had regional metastases: 2 had nodal disease confirmed after the operation, and 2 who had had no pathological sign of disease in the neck, developed regional recurrence. The authors reported a recurrence rate of 11% compared with 12% in other reports, and they concluded that there was no evidence that elective SND results in better disease control.41 Brown et al also reported that neck dissection is not required for SCC of the maxillary sinus and that postoperative radiotherapy should always be considered. However, when free flap reconstruction is used, the neck is usually accessed for the anastomosis of vessels (although other sites such as the superficial temporal vessels can sometimes be used). In patients who do not have microvascular reconstruction (for example, when obturators or a temporalis flap is used), or neck dissection, it could lead to under-staging of the neck.40 Neck dissection after chemoradiotherapy for mucosal SCC of the head and neck An elective neck dissection may be beneficial for patients with persistent or recurrent resectable disease in the neck after chemoradiotherapy.42 However, the therapeutic effects of chemoradiotherapy continue long after treatment, and the sampling of cervical lymph nodes may produce falsepositive results for many weeks or even months.43 The optimal time for assessing response as identified by computed tomography (CT), magnetic resonance imaging (MRI), or positron emission tomography (PET)-CT, is 8 -12 weeks after chemoradiotherapy.44 It had been thought that delaying the operation for more than 12 weeks reduces disease control in the neck, but the evidence is not entirely clear.45 In a review, Ferlito et al evaluated the necessity of planned neck dissection in patients who responded completely to chemoradiotherapy.46 A total of 24 studies showed that neck dissection gave an advantage, and among them, regional
failures varied from 0 - 38%. However, in 26, elective neck dissection was not advantageous. Most of the studies reported regional failure rates of between 0 and 16%, which are comparable to those of elective neck dissection. PET-CT may help to detect persistent or recurrent disease in the neck, and an elective neck dissection in patients with a complete response to chemoradiotherapy after 12 weeks would be difficult to justify.47,48 Evidence is emerging that, when clinically possible, SND can be done after chemoradiotherapy in most patients.49,50 However, the results included patients with bulky neck disease who had, and had not had, a complete response to chemoradiotherapy. A total of 62 patients had 69 operations (SND), and in most, residual disease was confined to levels II and III. Robbins et al explored the feasibility of SSND after chemoradiotherapy. Initially, the data were based on 177 patients (with clinically involved necks) who had concomitant chemotherapy and radiotherapy, and comparisons were made between those with disease in specific levels when it was restaged after chemotherapy, and the evidence of pathological disease. In those whose necks were restaged as a “partial response”, 73 had evidence of residual lymphadenopathy at one level. A total of 57 patients had salvage neck dissection and 2 had evidence of disease that extended beyond one level. This raises the possibility that SSND can be done if residual nodal disease is confined to a single level.51 In another study, Robbins et al included 241 patients with stage IV SCC of the head and neck who had had SND, SSND, or radical or MRND, and found that SSND was effective in a subgroup of patients after chemoradiotherapy. It could be seen as an adjuvant, as opposed to primary treatment, and is based on the principle that levels with no clinical sign of metastases before treatment had a therapeutic dose of radiation plus chemotherapy, which would obviate the need for them to be removed despite there being signs of disease in other levels. It must be remembered that lymphatic drainage changes unpredictably after surgical or non-surgical oncological treatment of the neck. However, if SND or SSND is done, in 20% of cases the internal jugular vein, sternocleidomastoid, or spinal accessory nerve is removed for adequate resection.52,53 Sentinel lymph node biopsy (SLNB) The use of SLNB has become established for early oral cancer and has been recommended as an alternative to neck dissection in patients with T1-T2 N0 disease.54,55 Gurney et al suggested that it can be used to identify different prognostic groups, which would allow better tailoring of treatment, and enable more focused management of the neck.56 It has also been identified as the most cost-effective procedure in the management of N0 in early oral cancer.57,58 It can accurately detect occult metastases and has good long-term disease control at the site affected in patients who have the procedure alone,59 and also causes less postoperative morbidity than
Please cite this article in press as: Green B, et al. Current surgical management of metastases in the neck from mucosal squamous cell carcinoma of the head and neck. Br J Oral Maxillofac Surg (2015), http://dx.doi.org/10.1016/j.bjoms.2015.06.025
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elective neck dissection. 60 Flach et al found that SLNB reduced the risk of occult metastases from 40% to 8% in patients with T1/T2 oral SCC. 61 When sentinel nodes were not involved, control in the neck was 97%; when they were involved it was 95%. Den Toom et al found that SLNB had a sensitivity of 93%, and advocated its use primarily for T1/T2 oral SCC.62 It can also be used as a safe and accurate method of staging to select patients with clinically stage I/II oropharyngeal SCC and occult lymph node metastases for elective neck dissection,63 and in patients with carcinoma of the floor of the mouth.64 Some advocate its use in patients who have previously had the neck treated. However, the rate of detection varies and depends on whether they had ipsilateral, contralateral, or bilateral neck dissection. Despite this, it can also be useful in the assessment of individual lymphatic drainage patterns.65 Excellent control in the neck, which compares well with elective neck dissection, can be achieved in patients who have not had a neck dissection and have no sign of disease on SLNB.56 Conclusion There seems to be an interest in super selective neck dissection, and with advances in diagnostic imaging (including SLNB and PET-CT) the tailoring of individual treatment plans for the neck is likely to become the next major development. Conflict of Interest We have no conflicts of interest
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Please cite this article in press as: Green B, et al. Current surgical management of metastases in the neck from mucosal squamous cell carcinoma of the head and neck. Br J Oral Maxillofac Surg (2015), http://dx.doi.org/10.1016/j.bjoms.2015.06.025
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Please cite this article in press as: Green B, et al. Current surgical management of metastases in the neck from mucosal squamous cell carcinoma of the head and neck. Br J Oral Maxillofac Surg (2015), http://dx.doi.org/10.1016/j.bjoms.2015.06.025