Best Practice & Research Clinical Endocrinology & Metabolism
Volume 22, Issue 6 , Pages 971-987 , December 2008

Surgical approaches in thyroid cancer and lymph-node metastases

  • Henning Dralle, MD (Professor and Chairman)
  • ,
  • Andreas Machens, MD (Associate Professor)

      Affiliations

    • Corresponding Author InformationCorresponding author. Tel.: +49 345 557 2314; Fax: +49 345 557 2551.

References 

  1. British Thyroid Association . Guidelines for the management of thyroid cancer in adults. Available from: http://www.british-thyroid-association.org
  2. Dralle H. Evidence-based endocrine surgery: thyroid cancer. Editorial World Journal of Surgery. 2007;31:877–878
  3. Machens A, Hauptmann S, Dralle H. Referral bias in thyroid cancer surgery: direction and magnitude. European Journal of Surgical Oncology. 2008;34:556–562
  4. Cady B, Rossi R. An expanded view of risk-group definition in differentiated thyroid carcinoma. Surgery. 1988;104:947–953
  5. Shaha A, Loree TR, Shah JP. Intermediate-risk group for differentiated carcinoma of thyroid. Surgery. 1994;116:1036–1041
  6. Lang BHH, Chow SM, Lo CY, et al. Staging systems for papillary thyroid carcinoma. Annals of Surgery. 2007;246:114–121
  7. In:  Sobin LH,  Ch Wittekind editor. TNM classification of malignant tumors. 6th edn.. Wiley-Liss, Inc.; 2002;
  8. Davies L, Welch HG. Increasing incidence of thyroid cancer in the United States, 1973–2002. JAMA: The Journal of the American Medical Association. 2006;296:2164–2167
  9. Pacini F, Ladensohn PW, Schlumberger M, et al. Radioiodine ablation of thyroid remnants after preparation with recombinant human thyrotropin in differentiated thyroid carcinoma: results of an international, randomized, controlled study. The Journal of Clinical Endocrinology and Metabolism. 2006;91:926–932
  10. Thomusch O, Sekulla C, Walls G, et al. Analysis of surgery-related complications in thyroid carcinoma - a German prospective multicentre study with 275 patients. Acta Medica Austriaca. 2001;33:194–198
  11. Udelsman R, Lakatos E, Ladenson P. Optimal surgery for papillary thyroid carcinomas. World Journal of Surgery. 1996;20:88–93
  12. Cooper DS, Doherty GM, Haugen BR, et al. Management guidelines for patients with thyroid nodules and differentiated thyroid cancer. Thyroid. 2006;16:1–33
  13. Dutch Association of Comprehensive Cancer Centres Thyroid Cancer . National evidence-based guideline. Available from: http://www.oncoline.nl
  14. Pacini F, Schlumberger M, Dralle H, et al. European consensus for the management of patients with differentiated thyroid carcinoma of the follicular epithelium. European Journal of Endocrinology. 2006;154:787–803
  15. Bilimoria KY, Bentrem DJ, Ko CY, et al. Extent of surgery affects survival for papillary thyroid cancer. Annals of Surgery. 2007;246:375–384
  16. Passler C, Scheuba C, Asari R, et al. Importance of tumor size in papillary and follicular thyroid cancer. The British Journal of Surgery. 2005;92:184–189
  17. LiVolsi VA, Mozzaferri EL, Schneider AB, et al. Papillary carcinoma. In:  DeLellis RA,  Lloyd RV,  Heitz PU, et al. editor. Tumours of endocrine organs. Pathology and genetics. World Health Organization classification of tumours. Lyon: IARC Press; 2004;p. 57–66
  18. Sobrinho-Simoes M, Noguchi SU, Mazzaferri EL, et al. In:  DeLellis RA,  Lloyd RV,  Heitz PU editor. Tumours of endocrine organs. Pathology and genetics. World Health Organization classification of tumours. Lyon: IARC Press; 2004;p. 67–72
  19. Schmid KW, Farid NR. How to define follicular thyroid carcinoma?. Virchows Archiv. 2006;448:385–393
  20. Schmid KW, Tötsch M, Öfner D, et al. Minimally invasive follicular thyroid carcinoma: a clinico-pathological study. In:  Schmid KW,  Böcker W editor. Thyroid pathology. Berlin: Springer; 1997;p. 37–43
  21. Brennan MD, Bergstralh EJ, v Heerden JA, et al. Follicular thyroid cancer treated at the Mayo clinic 1946 through 1970: initial manifestions, pathologic, findings, therapy, and outcome. Mayo Clinic Proceedings. 1991;66:11–22
  22. van Heerden JA, Hay ID, Goellner JR, et al. Follicular thyroid carcinoma with capsular invasion alone: a nonthreatening malignancy. Surgery. 1992;112:1130–1138
  23. Davis NL, Bugis SP, McGregor GI, et al. An evaluation of prognostic scoring systems in patients with follicular thyroid cancer. American Journal of Surgery. 1995;170:476–480
  24. DeGroot LJ, Kaplan EL, Shukla MS, et al. Morbidity and mortality in follicular thyroid cancer. The Journal of Clinical Endocrinology and Metabolism. 1995;80:2946–2953
  25. Shaha AR, Loree TR, Shah JP. Prognostic factors and risk group analysis in follicular carcinoma of the thyroid. Surgery. 1995;118:1131–1138
  26. Rao RS, Parikh HK, Deshmane VH, et al. Prognostic factors in follicular carcinoma of the thyroid: a study of 198 cases. Head & Neck. 1996;18:118–126
  27. Saadi H, Kleidermacher P, Esselstyn C. Conservative management of patients with intrathyroidal well-differentiated follicular thyroid carcinoma. Surgery. 2001;130:30–35
  28. Chow SM, Law SCK, Mendenhall WM, et al. Follicular thyroid carcinoma. Cancer. 2002;95:488–498
  29. Witte J, Goretzki PE, Diaken J, et al. Importance of lymph node metastases in follicular thyroid cancer. World Journal of Surgery. 2002;26:1017–1022
  30. D'Avanzo A, Treseler P, Ituarte PHG, et al. Follicular thyroid carcinoma: histology and prognosis. Cancer. 2004;100:1123–1129
  31. Furlan JC, Bedard YC, Rosen IB. Clinicopathologic significance of histologic vascular invasion in papillary and follicular thyroid carcinoma. Journal of the American College of Surgeons. 2004;198:341–348
  32. Passler C, Scheuba C, Prager G, et al. Prognostic factors of papillary and follicular cancer: differences in an iodine-replete endemic goiter region. Endocrine-Related Cancer. 2004;11:131–139
  33. Besic N, Zgajnar J, Hocevar M, et al. Is patients' age a prognostic factor for follicular thyroid carcinoma in the TNM classification system?. Thyroid. 2005;15:439–448
  34. Lo CY, Chan WF, Lam KY, et al. Follicular thyroid carcinoma. The role of histology and staging systems in predicting survival. Annals of Surgery. 2005;242:708–715
  35. Furlan JC, Bedard YC, Rosen IB. Significance of tumor capsular invasion in well-differentiated thyroid carcinomas. The American Surgeon. 2007;73:484–491
  36. Shaha A. Invited commentary: minimally invasive follicular thyroid carcinoma. Surgery. 2001;130:119–120
  37. Delbridge L, Barraclough B, Parkyn R, et al. Minimally invasive follicular thyroid carcinoma: completion thyroidectomy or not?. ANZ Journal of Surgery. 2002;72:844–845
  38. Farahati J, Reiners Ch, Demidchik EP. Is the UICC/AJCC classification of primary tumor in childhood thyroid carcinoma valid?. Journal of Nuclear Medicine. 1999;40:2125
  39. Leboulleux S, Baudin E, Hartl D, et al. Follicular cell-derived thyroid cancer in children. Hormone Research. 2005;63:145–151
  40. Elisei R, Bottici V, Luchetti F, et al. Impact of routine measurement of serum calcitonin on the diagnosis and outcome of medullary thyroid cancer: experience in 10.894 patients with nodular thyroid disorders. The Journal of Clinical Endocrinology and Metabolism. 2004;89:163–168
  41. Miyauchi A, Matsuzuka F, Hivai K, et al. Unilateral surgery supported by germline RET oncogene mutation analysis in patients with sporadic medullary thyroid carcinoma. World Journal of Surgery. 2000;24:1367–1372
  42. Peix JL, Braun P, Saachat M, et al. Occult micro medullary thyroid carcinoma: therapeutic strategy and follow-up. World Journal of Surgery. 2000;24:1373–1376
  43. 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
  44. Machens A, Hinze R, Thomusch O, et al. Pattern of nodal metastasis for primary and reoperative thyroid cancer. World Journal of Surgery. 2002;26:22–28
  45. Machens A, Hinze R, Lautenschläger C, et al. Multivariate analysis of clinicopathologic parameters for the insular subtype of differentiated thyroid carcinoma. Archives of Surgery. 2001;136:941–944
  46. Hiltzik D, Carlson DL, Tuttle RM, et al. Poorly differentiated thyroid carcinomas defined on the basis of mitosis and necrosis. Cancer. 2006;106:1286–1295
  47. Pellegriti G, Giuffrida D, Scollo C, et al. Long-term outcome of patients with insular carcinomas of the thyroid. Cancer. 2002;95:2076–2085
  48. Machens A, Lautenschläger C, Thomusch O, et al. Extended surgery and early postoperative radiotherapy for undifferentiated thyroid carcinoma. Thyroid. 2001;11:373–380
  49. Lang BHH, Lo CY. Surgical options in undifferentiated thyroid carcinoma. World Journal of Surgery. 2007;31:969–977
  50. Machens A, Hinze R, Lautenschläger C, et al. Thyroid carcinoma invading the cervicovisceral axis: routes of invasion and clinical implications. Surgery. 2001;129:23–28
  51. Robbins KT, Medina JE, Wolfe GT, et al. Standardizing neck dissection terminology. Archives of Otolaryngology--Head & Neck Surgery. 1991;117:601–605
  52. Robbins KT, Clayman G, Levine PA, et al., the Committee for Head and Neck Surgery and Oncology, American Academy of Otolaryngology-Head and Neck Surgery  Neck dissection classification update. Archives of Otolaryngology--Head & Neck Surgery. 2002;128:751–758
  53. Qubain SW, Nakano S, Baba M, et al. Distribution of lymph node micrometastasis in pN0 well-differentiated thyroid carcinoma. Surgery. 2002;131:249–256
  54. Ch Wittekind, Greene FL, Henson DE, et al. TNM supplement. 3rd edn.. New York: Wiley-Liss; 2003;25–30
  55. Dralle H, Damm I, Scheumann GFW, et al. Compartment-oriented microdissection of regional lymph nodes in medullary thyroid carcinoma. Surgery Today. 1994;24:112–121
  56. Dralle H, Gimm O. Lymphadenektomie beim Schilddrüsenkarzinom. Der Chirurg. 1996;67:788–806
  57. Goropoulos A, Karamoshos K, Christodoulou A, et al. Value of the cervical compartments in the surgical treatment of papillary thyroid carcinoma. World Journal of Surgery. 2004;28:1275–1281
  58. Leboulleux S, Rubino C, Baudin E, et al. Prognostic factors for persistent or recurrent disease of papillary thyroid carcinoma with neck lymph node metastases and/or tumor extension beyond the thyroid capsule at initial diagnosis. The Journal of Clinical Endocrinology and Metabolism. 2005;90:5723–5729
  59. Ito Y, Jikuzono T, Higashiyama T, et al. Clinical significance of lymph node metastasis of thyroid papillary carcinoma located in one lobe. World Journal of Surgery. 2006;30:1821–1828
  60. Vasko V, Hu S, Wu G, et al. High prevalence and possible de novo formation of BRAF mutation in metastasized papillary thyroid cancer in lymph nodes. The Journal of Clinical Endocrinology and Metabolism. 2005;90:5265–5269
  61. Ito Y, Uruno T, Takamura Y, et al. Papillary microcarcinomas of the thyroid with preoperatively detectable lymph node metastasis show significantly higher aggressive characteristics on immuno-histochemical examination. Oncology. 2005;68:87–96
  62. Machens A, Holzhausen HJ, Lautenschläger C, et al. Enhancement of lymph node metastasis and distant metastasis of thyroid carcinoma. Cancer. 2003;98:712–719
  63. Scheumann GFW, Gimm O, Wegener G, et al. Prognostic significance and surgical management of locoregional lymph node metastases in papillary thyroid cancer. World Journal of Surgery. 1994;18:559–568
  64. Sugitani I, Kasai N, Fujimoto Y, et al. A novel classification system for patients with PTC: addition of the new variables of large (3 cm or greater) nodal metastases and reclassification during the follow-up period. Surgery. 2004;135:139–148
  65. Ito Y, Miyauchi A. Lateral and mediastinal lymph node dissection in differentiated thyroid carcinoma: indications, benefits, and risks. World Journal of Surgery. 2007;31:905–915
  66. White ML, Gauger PG, Doherty GM. Central lymph node dissection in differentiated thyroid cancer. World Journal of Surgery. 2007;31:895–904
  67. Ito Y, Tomoda C, Uruno T, et al. Clinical significance of metastasis to the central compartment from papillary microcarcinoma of the thyroid. World Journal of Surgery. 2006;30:91–99
  68. Wada N, Duh QY, Sugino K, et al. Lymph node metastasis from 259 papillary thyroid microcarcinomas. Annals of Surgery. 2003;237:399–407
  69. Pereira JA, Jimeno J, Miquel J, et al. Nodal yield, morbidity, and recurrence after central neck dissection for papillary thyroid carcinoma. Surgery. 2005;138:1095–1101
  70. Lee YS, Kim SW, Kang HS, et al. Extent of routine central lymph node dissection with small papillary thyroid carcinoma. World Journal of Surgery. 2007;31:1954–1959
  71. 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 Journal of Surgery. 2004;28:498–501
  72. Ito Y, Tomoda C, Uruno T, et al. Papillary microcarcinoma of the thyroid: how should it be treated?. World Journal of Surgery. 2004;28:1115–1121
  73. 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 Journal of Surgery. 2005;29:917–920
  74. Ito Y, Higashiyama T, Takamura Y, et al. Risk factors for recurrence to the lymph node in papillary thyroid carcinoma patients without preoperatively detectable lateral node metastasis: validity of prophylactic modified radical neck dissection. World Journal of Surgery. 2007;31:2085–2091
  75. Sywak M, Cornfod L, Roach P, et al. Routine ipsilateral level VI lymphadenectomy reduces postoperative thyroglobulin levels in papillary thyroid cancer. Surgery. 2006;140:1000–1007
  76. Henry JF, Gramatica L, Denizot A, et al. Morbidity of prophylactic lymph node dissection in the central neck area in patients with papillary thyroid carcinoma. Langenbeck’s Archives of Surgery. 1998;383:167–169
  77. Skinner MA, Moley JA, Dilley WG, et al. Prophylactic thyroidectomy in multiple endocrine neoplasia type 2A. The New England Journal of Medicine. 2005;353:1105–1113
  78. Roh JL, Park JY, Park CI. Total thyroidectomy plus neck dissection in differentiated papillary thyroid carcinoma patients. Annals of Surgery. 2007;245:604–610
  79. Cheah WK, Arici C, Ituarte PHG, et al. Complications of neck dissection for thyroid cancer. World Journal of Surgery. 2002;26:1013–1016
  80. Short SO, Kaplan JN, Laramore GE, et al. Shoulder pain and function after neck dissection with or without preservation of the spinal accessory nerve. American Journal of Surgery. 1984;148:478–482
  81. Dralle H, Scheumann GFW, Hundeshagen H, et al. Die transsternale zervikomediastinale Primärtumorresektion und Lymphadenektomie beim Schilddrüsenkarzinom. Langenbeck’s Archives of Surgery. 1992;377:34–44
  82. Sugenoya A, Asanuma K, Shingu K, et al. Clinical evaluation of upper mediastinal dissection for differentiated thyroid carcinoma. Surgery. 1993;113:541–544
  83. Feind CR, Cole RM. Contralateral spread of head and neck cancer. American Journal of Surgery. 1969;118:660–665
  84. Lam KYA, Yau Lo C. Diffuse sclerosing variant of papillary carcinoma of the thyroid: a 35-year comparative study at a single institution. Annals of Surgery Oncology. 2006;13:176–181
  85. Sanders LE, Silverman M. Follicular and Hürthle cell carcinoma: predicting outcome and directing therapy. Surgery. 1998;124:967–974
  86. Haigh PI, Urbach DR. The treatment and prognosis of Hürthle cell follicular thyroid carcinoma compared with its non-Hürthle cell counterpart. Surgery. 2005;138:1152–1158
  87. Sobrinho-Simoes M, Albores-Saavedra J, Tallini G, et al. Poorly differentiated carcinoma. Pathology and Genetics of Tumors of Endocrine Organs. In:  DeLellis R editors. RV Lloyd, PU Heitz, C Eng. Lyon: IARC Press; 2004;p. 73
  88. Pulcrano M, Boukheris H, Talbot M, et al. Poorly differentiated follicular thyroid carcinoma: prognostic factors and relevance of histological classification. Thyroid. 2007;17:639–646
  89. Kebebew E, Greenspan FS, Clark OH, et al. Anaplastic thyroid carcinoma. Cancer. 2005;103:1330–1335
  90. Machens A, Schneyer U, Holzhausen HJ, et al. Prospects of remission in medullary thyroid carcinoma according to basal calcitionin level. The Journal of Clinical Endocrinology and Metabolism. 2005;90:2029–2034
  91. Schlumberger MJ. Papillary and follicular thyroid carcinoma. The New England Journal of Medicine. 1998;338:297–306
  92. Machens A, Hofmann C, Hauptmann S, et al. Locoregional recurrence and death from medullary thyroid carcinoma in a contemporaneous series: 5-year results. European Journal of Endocrinology. 2007;157:85–93
  93. Kebebew E, Greenspan FS, Clark OH, et al. Extent of disease and practice patterns for medullary thyroid cancer. Journal of the American College of Surgeons. 2005;200:890–896
  94. Moley JF, Fialkowski EA. Evidence-based approach to the management of sporadic medullary thyroid carcinoma. World Journal of Surgery. 2007;31:946–956
  95. Modigliani E, Cohen R, Campos JM, et al., the GETC Study Group  Prognostic factors for survival and for biochemical cure in medullary thyroid carcinoma: results in 899 patients. Clinical Endocrinology. 1998;48:265–273
  96. Scollo C, Baudin E, Travagli JP, et al. Rationale for central und bilateral lymph node dissection in sporadic and hereditary medullary thyroid cancer. The Journal of Clinical Endocrinology and Metabolism. 2003;88:2070–2075
  97. Machens A, Hauptmann S, Dralle H. Prediction of lateral lymph node metastases in medullary thyroid cancer. The British Journal of Surgery. 2008;95:586–591
  98. Machens A, Hauptmann S, Dralle H. Increased risk of lymph node metastasis in multifocal hereditary and sporadic medullary thyroid cancer. World Journal of Surgery. 2007;31:1960–1965
  99. Machens A, Holzhausen HJ, Dralle H. Prediction of mediastinal lymph node metastasis in medullary thyroid carcinoma. The British Journal of Surgery. 2004;91:709–712
  100. Machens A, Holzhausen HJ, Dralle H. Contralateral cervical and mediastinal lymph node metastasis in medullary thyroid cancer: systemic disease?. Surgery. 2006;139:28–32
  101. Dralle H, Scheumann GFW, Proye C, et al. The value of lymph node dissection in hereditary medullary thyroid carcinoma: a retrospective, European, multicentric study. Journal of Internal Medicine. 1995;238:357–361
  102. Machens A, Niccoli-Sire P, Hoegel J, et al. Early malignant progression of hereditary medullary thyroid carcinoma. The New England Journal of Medicine. 2003;349:1517–1525
  103. Machens A, Ukkat J, Brauckhoff M, et al. Advances in the management of hereditary medullary thyroid cancer. Journal of Internal Medicine. 2005;257:50–59
  104. Niccoli-Sire P, Murat A, Rohmer V, et al. French Calcitonin Tumors Study Group (GETC). Familial medullary thyroid carcinoma with noncysteine RET mutations: phenotype-genotype relationship in a large series of patients. The Journal of Clinical Endocrinology and Metabolism. 2001;86:3746–3753
  105. Dralle H, Gimm O, Simon D, et al. Prophylactic thyroidectomy in 75 children and adolescents with hereditary medullary thyroid carcinoma: German and Austrian experience. World Journal of Surgery. 1998;22:744–751
  106. Ukkat J, Lorenz K, Hinze R, et al. Importance of early screening and prophylactic thyroidectomy in asymptomatic nonindex RET germline carriers. World Journal of Surgery. 2001;25:713–717
  107. Gimm O, Ukkat J, Niederle BE, et al. Timing and extent of surgery in patients with familial medullary thyroid carcinoma/multiple endocrine neoplasia 2A-related RET mutations not affecting codon 634. World Journal of Surgery. 2004;28:1312–1316
  108. Yip L, Cote GJ, Shapiro SE, et al. Multiple endocrine neoplasia type 2. Archives of Surgery. 2003;138:409–416
  109. Brandi ML, Gagel RF, Angeli A, et al. Consensus. Guidelines for diagnosis and therapy of MEN type 1 and type 2. The Journal of Clinical Endocrinology and Metabolism. 2001;86:5658–5671
  110. Moley JF, Wells SA, Dilley WG, et al. Reoperation for recurrent or persistent medullary thyroid cancer. Surgery. 1993;114:1090–1096
  111. Gimm O, Dralle H. Reoperation in metastasizing medullary thyroid carcinoma: is a tumor stage-oriented approach justified?. Surgery. 1997;122:1124–1131
  112. Gimm O, Ukkat J, Dralle H. Determinative factors of biochemical cure after primary and reoperative surgery for sporadic medullary thyroid carcinoma. World Journal of Surgery. 1998;22:562–568
  113. Chen H, Robert JR, Ball DW, et al. Effective long-term palliation of symptomatic, incurable metastatic medullary thyroid cancer by operative resection. Annals of Surgery. 1998;227:887–895
  114. Machens A, Gimm O, Ukkat J, et al. Repeat mediastinal lymph-node dissection for palliation in advanced medullary thyroid carcinoma. Langenbeck’s Archives of Surgery. 1999;384:271–276
  115. Kouvaraki MA, Lee JE, Shapiro SE, et al. Preventable reoperations for persistent and recurrent papillary thyroid carcinoma. Surgery. 2004;136:1189–1191

PII: S1521-690X(08)00116-4

doi: 10.1016/j.beem.2008.09.018

Best Practice & Research Clinical Endocrinology & Metabolism
Volume 22, Issue 6 , Pages 971-987 , December 2008