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Management of lateral cervical metastases in papillary thyroid cancer: patterns of lymph node distribution.

Abstract

In this article we discuss the management of lateral cervical lymph node metastases in papillary thyroid cancer (PTC). We conducted a retrospective analysis of cases of PTC at our tertiary academic medical center involving 32 patients who underwent 39 neck dissections for the management of lateral cervical metastases from 2000 to 2007. Of these patients, 18 underwent primary neck dissections at the time of thyroidectomy after fine-needle aspiration biopsy confirmed the PTC. Secondary neck dissections for delayed metastases were performed in 14 patients who had previously undergone thyroidectomy for confirmed PTC. All 32 patients had positive nodes in at least one level. Our results highlight the high incidence of multilevel cervical metastasis associated with PTC and suggest the importance of including level II-B (submuscular recess) when performing a neck dissection; the upper posterior triangle (level V-A) is less likely to harbor occult tumor. Lateral neck metastasis from PTC is common and predictable; locoregional control is improved with a formal, comprehensive neck dissection at the time of thyroidectomy.

Introduction

Papillary thyroid cancer (PTC) will manifest regional cervical lymphatic metastases in as many as 25 to 80%

of cases. (1-12) The management of these metastases in PTC remains controversial. Multiple authors advocate an elective nodal dissection of the central neck compartment (level VI) at the time of thyroidectomy because of the high incidence of occult metastases, the possibility of more accurate pathologic tumor staging, and the increased risk to the recurrent laryngeal nerves and parathyroid glands if delayed central compartment dissection is performed. (7-13)

The best management approach for lateral cervical metastases in PTC remains unclear. While it is recognized that PTC has a high incidence of occult disease, the majority of patients will never manifest lateral cervical nodal involvement. Figure 1 shows the levels of lymph nodes in the neck region. In patients who present with clinically involved lateral cervical lymph nodes (levels II to V), most authors recommend a neck dissection (ND). (1,3,5,8,11,13) The type of ND performed can range from a super-selective ND (i.e., excision of a single nodal echelon) to a complete, comprehensive ND (levels II to V). (14,15)

Kupferman et al recently reported a clinical series that demonstrated metastatic involvement in level III nodes (57%), as well as involvement of levels II, IV, and V in 21 to 52% of specimens. (11) The authors recommended a comprehensive ND (levels II to V) given the high incidence of multilevel nodal metastases. This study made no distinction regarding levels II-B (submuscular recess) and level V-A in terms of metastatic lymph node distribution.

Recent reports of patients with squamous cell carcinoma of the larynx would suggest that certain lymph node levels (especially level II-B) may not require dissection, thus shortening operative time and minimizing potential morbidityto the spinal accessory nerve. (16) Several authors also have noted that the ability to eliminate the dissection of the upper jugular lymph nodes (levels II-B and V-A) may shorten operative time and minimize potential morbidity to the spinal accessory nerve. (8,9,16)

[FIGURE 1 OMITTED]

The purpose of this project was to assess the pattern of cervical lymph node metastases in PTC with an emphasis on lymph node distribution in the upper neck region (levels II-B and V-A). In particular, can the surgeon avoid dissection of levels II-B and V-A to avoid dissection of the spinal accessory nerve, yet still provide an oncologically sound clearance of occult cervical metastatic disease?

Patients and methods

This project consisted of a retrospective study designed to analyze lymph node distribution in patients diagnosed with PTC who underwent a ND from 2000 to 2007 under the supervision of one surgeon (F.R.M.). Patients were eligible for study analysis if they had a diagnosis of PTC (including the follicular variant) pathologically confirmed either by fine-needle aspiration (FNA) biopsy or previous thyroidectomy, and if they required a ND as part of the treatment plan. Patients with follicular or medullary thyroid cancer were not included in the analysis.

The study population consisted of two groups: (1) patients who underwent primary ND at the time of total thyroidectomy and (2) patients who had undergone a previous thyroidectomy and presented with delayed cervical metastases. The diagnosis of regional cervical metastases was based on clinical examination (palpable cervical lymphadenopathy) and a variety of imaging studies, including ultrasound, whole-body I-131 scanning, computed tomography, and magnetic resonance imaging (MRI). Radiographically suspicious lymph nodes then underwent FNA biopsy. Lymph node levels were defined according to the anatomic boundaries described in a recent update on classification of ND surgery. (15)

The majority of patients underwent a selective ND (levels II to V) with preservation of the sternocleidomastoid muscle, internal jugular vein, and spinal accessory nerve as dictated by operative findings. Level I lymph nodes were removed in selected cases in which preoperative imaging or operative findings indicated extension into level I nodes or structures. The specimens were oriented on the operative field by the senior surgeon and cut into individual specimens including levels II-A, II-B, III, IV, V-A, V-B, and level I (if removed).

All NDs were evaluated according to a protocol that has been previously described. Briefly, lymph nodes were meticulously removed from the specimen and measured in 3 dimensions. Either representative sections or the entire specimen was submitted for processing and preparation of histologic sections. One hematoxylin-eosin--stained glass slide was evaluated for each tissue block submitted. Additional levels were prepared as necessary. The total number of lymph nodes identified and the number and size of lymph nodes containing metastatic tumor were reported by anatomic level. Routine thyroglobulin staining was not performed.

Results

Thirty-two patients (13 men and 19 women; mean age 45 years [range: 19 to 72 years]) met the criteria as described above for entrance into this study. Eighteen patients underwent a total thyroidectomy with primary ND, and 14 had undergone previous thyroidectomy with delayed cervical metastasis at an average of 29 months post-thyroidectomy. Of the 18 patients who underwent primary ND, 7 underwent bilateral procedures, for a total of 39 NDs. All patients underwent NDs from levels II through V, and 6 of the 39 specimens included level I nodes. The final analysis of the 32 patients revealed 22 (69%) patients with a pathologic diagnosis of PTC, 4 (13%), with tall cell variants of PTC, and 6 (19%) with follicular variants of PTC. An average of 43 lymph nodes was obtained for each ND specimen.

[FIGURE 2 OMITTED]

The incidence of positive nodes for levels II through V are as follows: level IIA 49% (19/39); level IIB 62% (24/39); level III 72% (28/39); level IV 67% (26/39); level V-A 8% (3/39); level V-B 31% (12/39). In 3 of the 6 patients (50%) that underwent a level I lymph node dissection, the specimen contained metastatic disease. All patients who underwent primary ND and 13 of the 14 patients who underwent secondary ND had positive lymph nodes in at least one level. Overall, 72% (28/39) of all specimens contained metastatic disease in multiple lymph node levels.

Discussion

The definitive management of cervical metastases in PTC remains controversial. Historic data would suggest that clinically palpable or radiographically positive lymph nodes can be detected in as many as 20 to 40% of patients with PTC while as many as 80 to 90% of this same patient population may have occult nodal metastases. (3,5,8,11) In patients with no clinical/radiographic evidence of regional lymph node involvement, several authors have recommended elective central lymph node compartment dissection (level VI). The elective removal of the central lymph node compartment (first nodal echelon) is advocated based on the argument that it will remove any occult disease, provide definitive pathologic staging, lower the need for central neck revision surgery and, theoretically, improve locoregional control and long-term disease-free survival. (7,8,12,13) Occult metastatic disease in the lateral neck is common, but most authors agree that there is little role for elective lateral ND in the management of PTC. (5,6,8,11)

In patients who present with clinically or radiographically confirmed metastatic PTC in the lateral cervical compartment, the surgeon must decide on the appropriate lymph node levels to remove. Kupferman et al demonstrated a high incidence of metastatic disease in levels II and III (52 and 57%, respectively) and multilevel lymph node metastases in 68% of the patients. (11) Given these findings, the authors recommended a comprehensive ND of levels II to V for complete clearance of lateral cervical metastases. No breakdown of lymph node distribution to level II-A/II-B or V-A/V-B was provided.

Recent publications regarding patients with head and neck squamous cell carcinoma have shown a very low incidence of lymph node metastases to level II-B (submuscular recess). (16,17) Silverman et al reported an incidence of metastases to level II-B of 1.6% in clinically node-negative necks and 11.1% in clinically node-positive necks, with an overall incidence of 4.4%. (16) The primary tumor sites included the oral cavity, oropharynx, hypopharynx, and larynx. (16)

Dissection and removal of the level II-B lymph nodes requires an extensive dissection and mobilization of the proximal portion of the spinal accessory nerve (SAN). Traction injury and disruption of the blood supply to the SAN can result in significant postoperative shoulder dysfunction and pain. (16,17) We are not aware of any studies that have looked at the lymph node distribution in levels II- B and V-A in patients with well-differentiated thyroid cancer (WDTC). The obvious benefit of not having to dissect these levels is a quicker and simpler operation that may pose less risk of injury to the SAN.

Our data are in agreement with previously published reports in that the majority of cervical metastases in WDTC occur in levels II, III, and IV. In addition, we have demonstrated that multilevel lymph node metastasis is common (figure 2) and was seen in 72% of our ND specimens. This is also in agreement with previous reports in the literature. (1,5,10,11)

In addition to the high frequency of nodal metastases, we have demonstrated a high incidence of nodal metastases to level II-B (62%) and level V-B (31%). Simply removing a single node or even a nodal level may leave residual disease that might lead to the need for revision surgery and increased morbidity. The standard recommendations for the management of lateral cervical metastases are outlined in the National Comprehensive Cancer Network (NCCN) Clinical Practice Guidelines in Oncology and include removal of lymph node levels from levels II through W. (14)

It is obvious that PTC can undergo extensive multilevel occult lymph node metastases beyond the clinically apparent node. Therefore, we would recommend a formal comprehensive lymph node dissection to include levels II through V (including the level II-B lymph nodes).

References

(1.) Yanir Y, Doweck I. Regional metastases in well-differentiated thyroid carcinoma: Pattern of spread. Laryngoscope 2008;118(3):433-6.

(2.) Hughes CJ, Shaha AR, Shah JP, Loree TR. Impact of lymph node metastasis in differentiated carcinoma of the thyroid: A matched-pair analysis. Head Neck 1996;18(2): 127-32.

(3.) Watkinson JC, Franklyn JA, Olliff JF. Detection and surgical treatment of cervical lymph nodes in differentiated thyroid cancer. Thyroid 2006;16(2):187-94.

(4.) Dzodic R, Markovic I, Inic M, et al. Sentinel lymph node biopsy may be used to support the decision to perform modified radical neck dissection in differentiated thyroid carcinoma. World J Surg 2006;30(5):841-6.

(5.) Sivanandan R, Soo KC. Pattern of cervical lymph node metastases from papillary carcinoma of the thyroid. Br J Surg 2001;88(9): 1241-4.

(6.) Leong SP, Cady B, Iablons DM, et al. Clinical patterns of metastasis. Cancer Metastasis Rev 2006;25(2):221-32.

(7.) Shindo M, Wu JC, Park EE, Tanzella F. The importance of central compartment elective lymph node excision in the staging and treatment of papillary thyroid cancer. Arch Otolaryngology Head Neck Surg 2006;132(6):650-4.

(8.) Ferlito A, Pellitteri PK, Robbins KT, et al. Management of the neck in cancer of the major salivary glands, thyroid and parathyroid glands. Acta Otolaryngol 2002;122(6):673-8.

(9.) Ardito G, Rulli F, Revelli L, et al. A less invasive, selective, functional neck dissection for papillary thyroid carcinoma. Langebecks Arch Surg 2005;390(5):381-4.

(10.) Wada N, Duh QY, Sugino K, et al. Lymph node metastasis from 259 papillary thyroid microcarcinomas: Frequency, pattern of occurrence and recurrence, and optimal strategy for neck dissection. Ann Surg 2003;237(3):399-407.

(11.) Kupferman ME, Patterson M, Mandel SJ, et al. Patterns of lateral neck metastasis in papillary thyroid carcinoma. Arch Otolaryngol Head Neck Surg 2004;130(7):857-60.

(12.) Goropoulos A, Karamoshos K, Christodoulou A, et al. Value of the cervical compartments in the surgical treatment of papillary thyroid carcinoma. World J Surg 2004;28(12):1275-81.

(13.) Lee SH, Lee SS, Jin SM, et al. Predictive factors for central compartment lymph node metastasis in thyroid papillary microcarcinoma. Laryngoscope 2008;118(4):659-62.

(14.) National Comprehensive Cancer Network. Clinical Practice Guidelines in Oncology: Thyroid Cancer; 2007:2:1-68.

(15.) 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(5):536-8.

(16.) Silverman DA, El-Hajj M, Strome S, Esclamado RM. Prevelance of nodal metastases in the submuscular recess (level IIb) during selective neck dissection. Arch Otolaryngol Head Neck Surg 2003;129 (7):724-8.

(17.) Kraus DH, Rosenberg DB, Davidson BJ, et al. Supraspinal accessory lymph node metastases in supraomohyoid neck dissection. Am J Surg 1996;172(6):646-9.

J. Michael King, MD; Christian Corbitt, MD; Frank R. Miller, MD, FACS

From the Department of Otolaryngology-Head and Neck Surgery, University of Texas Health Science Center San Antonio.

Corresponding author: Frank R. Miller, MD, FACS, Department of Otolaryngology-Head and Neck Surgery, University of Texas Health Science Center San Antonio, 7703 Floyd Curl Dr., Mail Code 7777, San Antonio, TX 78229. Email: millerfr@uthscsa.edu

Previous presentation: The information in this article has been updated from its presentation as a poster at the 7th International Conference on Head and Neck Cancer; July 19-23, 2008; San Francisco, Calif.
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Title Annotation:ORIGINAL ARTICLE
Author:King, J. Michael; Corbitt, Christian; Miller, Frank R.
Publication:Ear, Nose and Throat Journal
Article Type:Clinical report
Geographic Code:1USA
Date:Aug 1, 2011
Words:2360
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