Because of the surgical ramifications of unilateral as opposed to bilateral involvement of the lateral neck, preoperative imaging plays a key role in clarifying the need for, the extent, and the nature (’curative’ versus ‘palliative’) of lateral neck surgery in the absence or presence of distant metastases. The higher is the index of suspicion for distant metastases, the more carefully lateral neck surgery must balance the oncologic benefit deriving from the procedure with the attendant surgical morbidity [11,12]. Although the surgical complications of central compartment dissection [13–18] are well characterized, the surgical morbidity resulting from lateral compartment dissection has rarely been analyzed in a systematic fashion [19,20]. Because of the renewed interest in lateral compartment surgery worldwide , it may be pertinent to review recent trends of surgical indications for lateral neck dissection in patients with papillary thyroid cancer (PTC) and medullary thyroid cancer (MTC). Important risk factors of surgical complications will be described that must be factored into treatment plans to dissect, or not dissect, the lateral neck compartment, and if so, the extent of that dissection. Exempt from this review are follicular and undifferentiated thyroid cancers, for which lymph node dissections are mostly palliative.
Careful analysis of the histopathological pattern of central and lateral lymph node metastases in PTC uncovered two avenues of lymphatic tumor cell dissemination to the ipsilateral neck:
All in all, contralateral are less common than ipsilateral lymph node metastases [23,25–27]. Recognized risk factors for contralateral involvement include a larger number of central lymph node metastases  and advanced tumor stage.
Preoperative imaging, typically high-resolution ultrasonography with or without fine needle aspiration cytology and determination of thyroglobulin concentrations in the washout, takes center stage in deciding on the surgical strategy for metastatic PTC [28–31]. Although unilateral and bilateral therapeutic lateral neck dissection with curative intent is widely recognized, prophylactic lateral neck dissection is controversial. To clear those occult lymph node metastases that are found in 15% of ultrasonography-negative patients , some practice guidelines advocate prophylactic lateral node dissection, whereas others do not for lack of evidence that prophylactic lymph node dissection improves cause-specific survival .
In light of these data, prophylactic lateral neck dissection is warranted for locoregional control in patients with clinically node-negative PTC when one or more of the following conditions are present (Table 1):
More research is needed to clarify whether the presence of multifocality, adverse histopathology, and advanced tumor stage warrants prophylactic lateral neck dissection.
Like PTC, MTC has a propensity for early invasion of lymphatic vessels but does not concentrate radioiodine and differs from PTC in many other ways:
Although preoperative ultrasonography has limited value for prediction of surgical cure or detection of metastatic nodes [41–43], many practice guidelines, including the American Thyroid Association (ATA) management guidelines , rely on this imaging modality to determine the need for ipsilateral or bilateral lateral dissection. To make this determination, preoperative basal calcitonin serum levels [45▪▪] may be more useful than preoperative ultrasonography or the number of central lymph node metastases . In 268 previously untreated patients with MTC, the ipsilateral and contralateral lateral neck was involved when basal calcitonin levels ranged between 20 and 200 pg/ml (normal limit <5–10 pg/ml) [45▪▪]. These data suggested that a central and ipsilateral lateral neck dissection may be adequate for patients with preoperative basal calcitonin levels of 200 pg/ml or less, whereas it may be prudent to consider a central and bilateral lateral neck dissection after that threshold has been crossed.
Controversy continues to surround the extent (unilateral versus bilateral) of lateral neck dissection for a disease that is frequently systemic at the time of presentation, enabling biochemical cure in no more than 60% of patients with node-negative and 10–20% of patients with node-positive MTC [3,34]. These issues are best addressed during the informed consent process, striking a balance between oncological benefit, surgical morbidity, and the inconvenience and costs of follow-up for persistent disease.
Several classification systems, delineating the anatomical borders of the central, lateral, and mediastinal compartments with the respective nodal groups, have been put forward [46–51], all of which have inherent strengths and weaknesses. Remarkably, all classification systems consistently define the common carotid artery as the landmark delimiting the lateral from the central neck compartment. Likewise, the clavicles and the right and left subclavian veins mark off the lateral compartment inferiorly. On the contrary, the lateral compartment is ill-defined superiorly and laterally, reflecting the lack of suitable anatomical landmarks in the submandibular and nuchal area of the neck .
Selective (’berry picking’) as opposed to systematic neck dissection is associated with higher rates of locoregional recurrence  and has been largely abandoned. Currently, most lateral compartment dissections routinely encompass levels II–V . A few studies with long-term follow-up assessed the need for removal of the lateral compartment in part or as a whole. In a retrospective study with a 4.5-year follow-up, Orlo Clark's group reported that not all patients with PTC required dissection of level I and V, decreasing the overall surgical complication rate . No such study has appeared for MTC as of this writing. Conceivably, sentinel lymph node biopsy may help determine the need for, and the extent of, lateral compartment dissection, but this proposition has not been evaluated in studies of sufficient duration [55,56]. At the moment, dissection of the complete lateral compartment, comprising levels II–V, represents the gold standard of lateral neck dissection. Nevertheless, for PTC in particular, further research is needed to define precisely those variations in lymphatic tumor spread that may allow, without worsening oncological outcome, a reduction in the extent of lateral dissection and surgical complications.
Lateral compartment dissection is not associated with fewer early and late surgical complications than central compartment dissection. Although injury to the recurrent laryngeal nerve and the parathyroid glands has been researched extensively, only a few studies have specifically dealt with the surgical morbidity of lateral neck dissection.
Owing to numerous posterior collaterals, the clearance of lateral neck nodes does not impair the lymphatic drainage of the neck. Nonetheless, lateral compartment dissection may give rise to two key complications that occur early and late after the operation: lymphatic leakage, and spinal accessory nerve damage resulting in shoulder dysfunction, which may be painful. Although less common, the cervical plexus, the sympathetic trunk, and phrenic, hypoglossal, and vagal nerves can also become subject to injury, usually during resection of locoregional disease or during extensive neck dissection. No data are available from the literature regarding frequency and socioeconomic burden entailed by these nerve injuries. Intriguingly, lateral (phrenic) and central neck (recurrent laryngeal) nerve palsies may work in synergy, causing serious respiratory problems. Carotid artery rupture, although rare, is almost invariably fatal. This life-threatening complication represents the catastrophic climax of a deep-seated wound infection in connection with a skeletonized carotid artery or previous neck irradiation [57,58].
After thyroidectomy and lateral neck dissection, chyle leakage is observed in 0.5–8% of patients [20,59–61], usually near the junction of the left subclavian and left internal jugular veins . Lymphatic leakage predisposes to infection of the neck wound and prolongs hospitalization. In our experience, the intraoperative use of milk-based solutions is not always suited to pinpoint the lymphatic leak inside the operative field. More helpful is the meticulous dissection of the entry of the thoracic duct into the venous angle using magnifying glasses. Lymphatic leaks should be ligated upon detection, avoiding the use of suture ligations that can tear the delicate wall of the leaking lymph vessel. Lymphatic leaks tend to appear on the first or second postoperative day or may not manifest clinically before the seventh postoperative day . There is still some conflict of opinion on whether postoperative lymphatic leaks are to be closed surgically or treated conservatively. Nevertheless, there is overwhelming support for the early surgical closure of high-output leaks as it emerges that conservative management is failing. If no lymphatic leak is identifiable on reexploration of the neck wound, it is our customary practice to seal the leaking area, covering it with a muscle flap.
Shoulder dysfunction due to spinal accessory nerve injury is thought to affect 25–50% of patients undergoing lateral neck dissection, depending on the extent of that dissection [20,63–65]. Unlike recurrent laryngeal nerve injury, which is quickly recognized clinically and through postoperative laryngoscopy, spinal accessory nerve injury starts out subtle and may take weeks to manifest fully, at which time the patient is no longer hospitalized. Specific neurological examinations are often necessary to make the diagnosis [63–65]. Accessory nerve dysfunction causes the trapezius muscle to weaken, diminishing shoulder abduction and flexion . Many patients with shoulder dysfunction and pain, struggling to resume their former activities of daily life, are unable to return to work . In the first 6 months after the operation, physiotherapy may facilitate the recovery of trapezius muscle function, after which time muscle strength is unlikely to recover further .
A review of the pertinent literature disclosed that the surgical risks of lateral compartment dissection for thyroid cancer are frequently underestimated. There is a dire need for more research using more sensitive detection methods so that the treatment of neurological deficits can be improved. In view of the socioeconomic ramifications of postoperative shoulder dysfunction, affecting as many as 67% of patients , and given the unavailability of effective therapies , the indication for, and the extent of lateral neck dissection for thyroid cancer must be scrutinized weighing oncologic benefits against surgical morbidity.
Lateral neck dissection for metastatic thyroid cancer, owing to the centrifugal orientation of the lymphatic system draining the thyroid gland, is a fairly common procedure. Tumors lodging in the upper thyroid pole may skip the central compartment, spreading directly to the superior lateral nodes (first basin), whereas tumors located in the inferior thyroid pole tend to involve both the central and the inferior lateral (supraclavicular) nodes (first basin). Contralateral lateral neck metastases, in particular in patients with MTC, are associated with mediastinal and distant metastases.
Although dissection of the lateral neck compartment is warranted for clinically involved lateral neck nodes, prophylactic lateral compartment dissections, giving rise to lateral nerve injuries more often than previously thought, should be limited to tumors originating from the upper thyroid pole or thyroid tumors with extensive involvement of the ipsilateral or bilateral central neck compartment. In patients with MTC and preoperative basal calcitonin levels more than 200 pg/ml, a central and bilateral lateral compartment dissection is needed, whereas a central and unilateral lateral compartment dissection would be adequate below that threshold.
Papers of particular interest, published within the annual period of review, have been highlighted as:
Additional references related to this topic can also be found in the Current World Literature section in this issue (p. 100).
1. Gimm O, Rath FW, Dralle H. Pattern of lymph node metastases in papillary thyroid carcinoma. Br J Surg 1998; 85:252–254.
2. Machens A, Hinze R, Thomusch O, Dralle H. Pattern of nodal metastasis for primary and reoperative thyroid cancer. World J Surg 2002; 26:22–28.
3. Machens A, Holzhausen HJ, Dralle H. Contralateral cervical and mediastinal lymph node metastasis in medullary thyroid cancer: systemic disease? Surgery 2006; 139:28–32.
4. Machens A, Hauptmann S, Dralle H. Prediction of lateral lymph node metastases in medullary thyroid cancer. Br J Surg 2008; 95:586–591.
5. Machens A, Holzhausen HJ, Dralle H. Prediction of mediastinal lymph node metastasis in medullary thyroid carcinoma. Br J Surg 2004; 91:709–712.
6. Machens A, Dralle H. Prediction of mediastinal lymph node metastasis in papillary thyroid cancer. Ann Surg Oncol 2009; 16:171–176.
7▪. Park JH, Lee YS, Kim BW, et al. Skip lateral neck node metastases in papillary thyroid carcinoma. World J Surg 2012; 36:743–747.
This study of 147 patients with papillary thyroid cancer found skip metastases in 32 patients (21.8%). Skip metastases occurred commonly with primary tumors of the upper pole, and with tumors of 1 cm or less in diameter.
8▪▪. Zhang L, Wei WJ, Ji QH, et al. Risk factors for neck metastasis in papillary thyroid carcinoma: a study of 1066 patients. J Clin Endocrinol Metab 2012; 97:1250–1257.
In this retrospective cross-sectional study of 1066 patients with papillary thyroid microcarcinoma, extrathyroidal extension, multifocal lesions, and central lymph node metastases were associated with lateral neck lymph node metastasis on multivariate logistic regression analysis. In patients with a solitary primary tumor, tumor location in the upper third of the thyroid lobe was associated with a lower risk of central lymph node metastasis and a higher risk of lateral neck lymph node metastasis.
9. Von Lanz T, Wachsmuth W. Praktische Anatomie, Hals [in German]. Berlin: Springer Verlag; 1955. pp. 243–244.
10. Földi M, Kubik S. Lehrbuch der Lymphologie [in German]. Fischer Verlag Stuttgart; 1989. pp. 27–50.
11. Evans DB. Papillary carcinoma of the thyroid: balancing principles of oncology with emerging technology. Surgery 2011; 150:1015–1022.
12. Cooper DS, Tufano RP. Prophylactic central neck dissection in differentiated thyroid cancer: a procedure in search of an indication. Thyroid 2012; 22:341–343.
13. Chisholm EJ, Kulinskaya E, Tolley NS. Systemic review and meta-analysis of the adverse effects of thyroidectomy combined with central neck dissection as compared with thyroidectomy alone. Laryngoscope 2009; 119:1135–1139.
14. Shen WT, Ogawa L, Ruan D, et al. Central neck lymph node dissection for papillary thyroid cancer: the reliability of surgeon judgment in predicting which patients will benefit. Surgery 2010; 148:398–403.
15. Hughes DT, White ML, Miller BS, et al. Influence of prophylactic central lymph node dissection on postoperative thyroglobulin levels and radioiodine treatment in papillary thyroid cancer. Surgery 2010; 148:1100–1107.
16. Moo TA, McGill J, Allendorf J, et al. Impact of prophylactic central neck lymph node dissection on early recurrence in papillary thyroid carcinoma. World J Surg 2010; 34:1187–1191.
17. Popadich A, Levin O, Lee JC, et al. A multicenter cohort study of total thyroidectomy and routine central lymph node dissection for cN0 papillary thyroid cancer. Surgery 2011; 150:1048–1057.
18. So YK, Seo MY, Son YI. Prophylactic central lymph node dissection for clinically node-negative papillary thyroid microcarcinoma: influence on serum thyroglobulin level, recurrence rate, and postoperative complications. Surgery 2012; 151:192–198.
19. Cheah WK, Arici C, Ituarte PHG, et al. Complications of neck dissection for thyroid cancer. World J Surg 2002; 26:1013–1016.
20. Kupferman ME, Patterson M, Mandel SJ, et al. Safety of modified radical neck dissection for differentiated thyroid carcinoma. Laryngoscope 2004; 114:403–406.
21. Palazzo FF, Gosnell J, Savio JGR, et al. Lymphadenectomy for papillary thyroid cancer: changes in practice over four decades. Eur J Surg Oncol 2006; 32:340–344.
22. Machens A, Holzhausen HJ, Dralle H. Skip metastases in thyroid cancer leaping the central lymph node compartment. Arch Surg 2004; 139:43–45.
23. Machens A, Hauptmann S, Dralle H. Lymph node dissection in the lateral neck for completion in central node-positive papillary thyroid cancer. Surgery 2009; 145:176–181.
24. Lee BJ, Lee JC, Wang SG, et al. Metastasis of right upper para-esophageal lymph nodes in central compartment lymph node dissection of papillary thyroid cancer. World J Surg 2009; 33:2094–2098.
25. Takada H, Kikumori T, Imai T, et al. Patterns of lymph node metastases in papillary thyroid carcinoma: results from consecutive bilateral cervical lymph node dissection. World J Surg 2011; 35:1560–1566.
26. Lim YS, Lee JC, Lee YS, et al. Lateral cervical lymph node metastases from papillary thyroid carcinoma: predictive factors of nodal metastasis. Surgery 2011; 150:116–121.
27. Ito Y, Kudo T, Takamura Y, et al. Lymph node recurrence in patients with N1b papillary thyroid carcinoma who underwent unilateral therapeutic modified radical neck dissection. World J Surg 2012; 36:593–597.
28. Ito Y, Tomoda C, Uruno T, et al. Preoperative ultrasonographic examination for lymph node metastasis: usefulness when designing lymph node dissection for papillary microcarcinoma of the thyroid. World J Surg 2004; 28:498–501.
29. Ito Y, Tomoda C, Uruno T, et al. Ultrasonographically and anatomopathologically detectable node metastases in the lateral compartment as indicators of worse relapse-free survival in patients with papillary thyroid carcinoma. World J Surg 2005; 29:917–920.
30. Caron NR, Tan YY, Ogilive JB, et al. Selective modified radical neck dissection for papillary thyroid cancer: is level I, II and V dissection always necessary? World J Surg 2006; 30:833–840.
31. Ito Y, Miyauchi A. Lateral and mediastinal lymph node dissection in differentiated thyroid carcinoma: indications, benefit, and risks. World J Surg 2007; 31:905–915.
32. Takami H, Ito Y, Okamoto T, Yoshida A. Therapeutic strategy for differentiated thyroid carcinoma in Japan based on a newly established guideline managed by Japanese Society of Thyroid Surgeons and Japanese Association of Endocrine Surgeons. World J Surg 2011; 35:111–121.
33. Machens A, Holzhausen HJ, Dralle H. The prognostic value of primary tumor size in papillary and follicular thyroid carcinoma. Cancer 2005; 103:2269–2273.
34. Machens A, Schneyer U, Holzhausen HJ, Dralle H. Prospects of remission in medullary thyroid carcinoma according to basal calcitonin level. J Clin Endocrinol Metab 2005; 90:2029–2034.
35▪▪. Machens A, Dralle H. Prognostic impact of N staging in 715 medullary thyroid cancer patients: proposal for a revised staging system. Ann Surg 2012. doi: 10.1097/SLA.0b013e318268301d.
In this study of 715 patients with MTC, extrathyroidal extension and one to 10 involved nodes indicated a small risk of lung metastasis [3–4%; odds ratio (OR) 3–4]; tumors more than 40 mm and 11–20 involved nodes implied an intermediate risk (13%; OR 6), and more than 20 involved nodes entailed a high risk (26–30%; OR 14–16). N categories encompassing 1–10 (N1), 11–20 (N2), and more than 20 (N3) lymph node metastases are important prognostic classifiers that should be incorporated into MTC staging systems for better risk stratification.
36. Kandil E, Gilson MM, Alabbas HH, et al. Survival implications of cervical lymphadenectomy in patients with medullary thyroid cancer. Ann Surg Oncol 2011; 18:1028–1034.
37. Machens A, Gimm O, Ukkat J, et al. Improved prediction of calcitonin normalization in medullary thyroid carcinoma patients by quantitative lymph node analysis. Cancer 2000; 88:1909–1915.
38. Kaserer K, Scheuba C, Neuhold N, et al. Sporadic versus familial medullary thyroid microcarcinoma: a histopathologic study of 50 consecutive patients. Am J Surg Pathol 2001; 25:1245–1251.
39. Scheuba C, Kaserer K, Kaczirek K, et al. Desmoplastic stromal reaction in medullary thyroid cancer: an intraoperative marker for lymph node metastases. World J Surg 2006; 69:312–316.
40. Koperek O, Scheuba C, Cherenko M, et al. Desmoplasia in medullary thyroid carcinoma: a reliable indicator of metastatic potential. Histopathology 2008; 52:623–630.
41. Moley JF, DeBenedetti MK. Patterns of nodal metastases in palpable medullary thyroid carcinoma: recommendations for extent of node dissection. Ann Surg 1999; 229:880–887.
42. Kebebew E, Kikichi S, Duh QY, Clark O. Long-term results of reoperation and localization studies in patients with persistent or recurrent medullary thyroid cancer. Arch Surg 2000; 135:895–901.
43. Kouvaraki MA, Shapiro SE, Fornage BD, et al. Role of preoperative ultrasonography in the surgical management of patients with thyroid cancer. Surgery 2003; 134:946–955.
44. Kloos RT, Eng C, Evans DB, et al. Medullary thyroid cancer: management guidelines of the American Thyroid Association. Thyroid 2009; 19:565–612.
45▪▪. Machens A, Dralle H. Biomarker-based risk stratification for previously untreated medullary thyroid cancer. J Clin Endocrinol Metab 2010; 95:2655–2663.
In this study of 300 patients with previously untreated medullary thyroid cancer, higher biomarker levels reflected larger primary tumors and more lymph node metastases. Stratified basal calcitonin serum levels correlated better (r = 0.59) with the number of lymph node metastases than carcinoembryonic antigen (r = 0.47) or pentagastrin-stimulated calcitonin (r = 0.40) levels. Lymph node metastases were present in the ipsilateral central and lateral neck, contralateral central neck, contralateral lateral neck, and upper mediastinum, respectively, beyond basal calcitonin thresholds of 20, 50, 200, and 500 pg/ml. Bilateral compartment-oriented neck surgery achieved biochemical cure in at least half the patients with pretherapeutic basal calcitonin levels of 1000 pg/ml or less but not in patients with levels greater than 10 000 pg/ml.
46. Qubain SW, Nakano S, Baba M, et al. Distribution of lymph node micrometastasis in pN0 well differentiated thyroid carcinoma. Surgery 2002; 131:249–256.
47. Dralle H, Damm I, Scheumann GFW, et al. Compartment-oriented microdissection of regional lymph nodes in medullary thyroid carcinoma. Surg Today 1994; 24:112–121.
48. Robbins KT, Shaha AR, Medina JE, et al. Consensus statement on the classification and terminology of neck dissection. Arch Otolaryngol Head Neck Surg 2008; 134:536–538.
49. Carty SE, Cooper DS, Doherty GM, et al. Consensus statement on the terminology and classification of central neck dissection for thyroid cancer. Thyroid 2009; 19:1153–1158.
50. Stack BC, Ferris RL, Goldenberg D, et al. American Thyroid Association consensus review and statement regarding the anatomy, terminology, and rationale for lateral neck dissection in differentiated thyroid cancer. Thyroid 2012; 22:501–508.
51. Wittekind C, Compton CC, Brierley J, Sobin LH. TNM supplement. A commentary on uniform use. 4th ed. Wiley-Blackwell; 2012.
52. Dralle H, Machens A. Surgical approaches in thyroid cancer and lymph-node metastases. Best Pract Res Clin Endocrinol Metab 2008; 22:971–987.
53. Musacchio MJ, Kim AW, Vijungco JD, Prinz RA. Greater local recurrence occurs with ‘berry picking’ than neck dissection in thyroid cancer. Am Surg 2003; 69:191–196.
54. Kupferman ME, Patterson M, Mandel SJ, et al. Patterns of lateral neck metastasis in papillary thyroid carcinoma. Arch Otolaryngol Head Neck Surg 2004; 130:851–860.
55. Balasubramanian SP, Harrison BJ. Systemic review and meta-analysis of sentinel node biopsy in thyroid cancer. Br J Surg 2011; 98:334–344.
56. Lee SK, Kim SH, Hur SM, et al. The efficacy of lateral neck sentinel lymph node biopsy in papillary thyroid carcinoma. World J Surg 2011; 35:2675–2682.
57. Maran AGD, Amin M, Wilson JA. Radical neck dissection: a 19-year experience. J Laryngol Otol 1989; 103:760–764.
58. Machens A, Dralle H. Mycotic aneurysm of common carotid artery induced by Staphylococcus aureus
infection after cervical reoperation. World J Surg 2001; 25:1113–1116.
59. Spiro JD, Spiro RH, Strong EW. The management of chyle fistula. Laryngoscope 1990; 100:771–774.
60. Roh JL, Kim DH, Park CI. Prospective identification of chyle leakage in patients undergoing lateral neck dissection for metastatic thyroid cancer. Ann Surg Oncol 2008; 15:424–429.
61. Lorenz K, Abuazab M, Sekulla C, et al. Management of lymph fistulas in thyroid surgery. Langenbecks Arch Surg 2010; 395:911–917.
62. Wu G, Chang X, Xia Y, et al.
Prospective randomized trial of high versus low negative pressure suction in management of chyle fistula after neck dissection for metastatic thyroid carcinoma. Head Neck 2012. doi: 10.1002/hed.21979.
63. Leipzig B, Suen JY, English JL, et al. Functional evaluation of the spinal accessory nerve after neck dissection. Am J Surg 1983; 146:526–530.
64. Sobol S, Jensen C, Sawyer W, et al. Objective comparison of physical dysfunction after neck dissection. Am J Surg 1985; 150:503–509.
65. Remmler D, Byers R, Scheetz J, et al. A prospective study of shoulder disability resulting from radical and modified neck dissections. Head Neck Surg 1986; 8:280–286.
66. McGarvey AC, Chiarelli PE, Osmotherly PG, Hoffmann GR. Physiotherapy for accessory nerve shoulder dysfunction following neck dissection surgery: a literature review. Head Neck 2011; 33:274–280.
67. Schuller DE, Reiches NA, Hamaker RC, et al. Analysis of disability resulting from treatment including radical neck dissection or modified neck dissection. Head Neck Surg 1983; 6:551–558.
68. van Wilgen CP, Dijkstra PU, van der Laan BF, et al. Shoulder complaints after nerve sparing neck dissections. Int J Oral Maxillofac Surg 2004; 33:253–527.