Surgery
Volume 148, Issue 3 , Pages 516-525 , September 2010

Indeterminate thyroid nodules: A challenge for the surgical strategy

  • Reza Asari, MD

      Affiliations

    • Section of Endocrine Surgery, Division of General Surgery, Department of General Surgery, Medical University of Vienna, Vienna, Austria
    • Corresponding Author InformationReprint requests: Reza Asari, MD, Section of Endocrine Surgery, Division of General Surgery, Department of General Surgery, Medical University of Vienna, Waehringer Guertel 18-20, 1080 Vienna, Austria.
  • ,
  • Barbara E. Niederle, MD

      Affiliations

    • Section of Endocrine Surgery, Division of General Surgery, Department of General Surgery, Medical University of Vienna, Vienna, Austria
  • ,
  • Christian Scheuba, MD

      Affiliations

    • Section of Endocrine Surgery, Division of General Surgery, Department of General Surgery, Medical University of Vienna, Vienna, Austria
  • ,
  • Philipp Riss, MD

      Affiliations

    • Section of Endocrine Surgery, Division of General Surgery, Department of General Surgery, Medical University of Vienna, Vienna, Austria
  • ,
  • Oskar Koperek, MD

      Affiliations

    • Department of Clinical Pathology, Medical University of Vienna, Vienna, Austria
  • ,
  • Klaus Kaserer, MD

      Affiliations

    • Department of Clinical Pathology, Medical University of Vienna, Vienna, Austria
  • ,
  • Bruno Niederle, MD

      Affiliations

    • Section of Endocrine Surgery, Division of General Surgery, Department of General Surgery, Medical University of Vienna, Vienna, Austria

,Accepted 21 January 2010.

References 

  1. Baloch ZW, Sack MJ, Yu GH, Livolsi VA, Gupta PK. Fine-needle aspiration of thyroid: an institutional experience. Thyroid. 1998;8:565–569
  2. Gharib H, Goellner JR, Johnson DA. Fine-needle aspiration cytology of the thyroid. A 12-year experience with 11,000 biopsies. Clin Lab Med. 1993;13:699–709
  3. Gharib H, Goellner JR. Fine-needle aspiration biopsy of the thyroid: an appraisal. Ann Intern Med. 1993;118:282–289
  4. Morgan JL, Serpell JW, Cheng MS. Fine-needle aspiration cytology of thyroid nodules: how useful is it?. ANZ J Surg. 2003;73:480–483
  5. Passler C, Prager M, Scheuba C, Kaserer K, Flores JA, Vierhapper H, et al. [The value of fine-needle aspiration biopsy (FNAB) in the differential diagnosis of the “cold” thyroid nodule]. Wien Klin Wochenschr. 1999;111:240–245
  6. Rojeski MT, Gharib H. Nodular thyroid disease. Evaluation and management. N Engl J Med. 1985;313:428–436
  7. Kopald KH, Layfield LJ, Mohrmann R, Foshag LJ, Giuliano AE. Clarifying the role of fine-needle aspiration cytologic evaluation and frozen section examination in the operative management of thyroid cancer. Arch Surg. 1989;124:1201–1204
  8. Alexander EK. Approach to the patient with a cytologically indeterminate thyroid nodule. J Clin Endocrinol Metab. 2008;93:4175–4182
  9. Baloch ZW, Cibas ES, Clark DP, Layfield LJ, Ljung BM, Pitman MB, et al. The National Cancer Institute Thyroid fine needle aspiration state of the science conference: a summation. Cytojournal. 2008;5:6
  10. Chen H, Nicol TL, Udelsman R. Follicular lesions of the thyroid. Does frozen section evaluation alter operative management?. Ann Surg. 1995;222:101–106
  11. Gharib H, Goellner JR, Zinsmeister AR, Grant CS, Van Heerden JA. Fine-needle aspiration biopsy of the thyroid. The problem of suspicious cytologic findings. Ann Intern Med. 1984;101:25–28
  12. Goldstein RE, Netterville JL, Burkey B, Johnson JE. Implications of follicular neoplasms, atypia, and lesions suspicious for malignancy diagnosed by fine-needle aspiration of thyroid nodules. Ann Surg. 2002;235:656–662
  13. McHenry CR, Thomas SR, Slusarczyk SJ, Khiyami A. Follicular or Hurthle cell neoplasm of the thyroid: can clinical factors be used to predict carcinoma and determine extent of thyroidectomy?. Surgery. 1999;126:798–802
  14. Monzani F, Caraccio N, Iacconi P, Faviana P, Dardano A, Basolo F, et al. Prevalence of cancer in follicular thyroid nodules: is there still a role for intraoperative frozen section analysis?. Thyroid. 2003;13:389–394
  15. Schmid KW, Hofstadter F, Propst A, Ladurner D, Zechmann W. A fourteen year practice with the fine needle aspiration biopsy of the thyroid in an endemic area. Pathol Res Pract. 1986;181:308–310
  16. Udelsman R. Thyroid cancer surgery. Rev Endocr Metab Disord. 2000;1:155–163
  17. Blansfield JA, Sack MJ, Kukora JS. Recent experience with preoperative fine-needle aspiration biopsy of thyroid nodules in a community hospital. Arch Surg. 2002;137:818–821
  18. Baloch ZW, Fleisher S, LiVolsi VA, Gupta PK. Diagnosis of “follicular neoplasm”: a gray zone in thyroid fine-needle aspiration cytology. Diagn Cytopathol. 2002;26:41–44
  19. Layfield LJ, Reichman A, Bottles K, Giuliano A. Clinical determinants for the management of thyroid nodules by fine-needle aspiration cytology. Arch Otolaryngol Head Neck Surg. 1992;118:717–721
  20. Raber W, Kaserer K, Niederle B, Vierhapper H. Risk factors for malignancy of thyroid nodules initially identified as follicular neoplasia by fine-needle aspiration: results of a prospective study of one hundred twenty patients. Thyroid. 2000;10:709–712
  21. Rago T, Di Coscio G, Basolo F, Scutari M, Elisei R, Berti P, et al. Combined clinical, thyroid ultrasound and cytological features help to predict thyroid malignancy in follicular and Hupsilonrthle cell thyroid lesions: results from a series of 505 consecutive patients. Clin Endocrinol. 2007;66:13–20
  22. Schlinkert RT, van Heerden JA, Goellner JR, Gharib H, Smith SL, Rosales RF, et al. Factors that predict malignant thyroid lesions when fine-needle aspiration is “suspicious for follicular neoplasm”. Mayo Clin Proc. 1997;72:913–916
  23. Sippel RS, Elaraj DM, Khanafshar E, Kebebew E, Duh QY, Clark OH. Does the presence of additional thyroid nodules on ultrasound alter the risk of malignancy in patients with a follicular neoplasm of the thyroid?. Surgery. 2007;142:851–857
  24. Tuttle RM, Lemar H, Burch HB. Clinical features associated with an increased risk of thyroid malignancy in patients with follicular neoplasia by fine-needle aspiration. Thyroid. 1998;8:377–383
  25. Tyler DS, Winchester DJ, Caraway NP, Hickey RC, Evans DB. Indeterminate fine-needle aspiration biopsy of the thyroid: identification of subgroups at high risk for invasive carcinoma. Surgery. 1994;116:1054–1060
  26. Wiseman SM, Baliski C, Irvine R, Anderson D, Wilkins G, Filipenko D, et al. Hemithyroidectomy: the optimal initial surgical approach for individuals undergoing surgery for a cytological diagnosis of follicular neoplasm. Ann Surg Oncol. 2006;13:425–432
  27. Brooks AD, Shaha AR, DuMornay W, Huvos AG, Zakowski M, Brennan MF, et al. Role of fine-needle aspiration biopsy and frozen section analysis in the surgical management of thyroid tumors. Ann Surg Oncol. 2001;8:92–100
  28. DeMay RM. Frozen section of thyroid?. Just say no. Am J Clin Pathol. 1998;110:423–424
  29. Hamburger JI, Hamburger SW. Declining role of frozen section in surgical planning for thyroid nodules. Surgery. 1985;98:307–312
  30. Keller MP, Crabbe MM, Norwood SH. Accuracy and significance of fine-needle aspiration and frozen section in determining the extent of thyroid resection. Surgery. 1987;101:632–635
  31. Mulcahy MM, Cohen JI, Anderson PE, Ditamasso J, Schmidt W. Relative accuracy of fine-needle aspiration and frozen section in the diagnosis of well-differentiated thyroid cancer. Laryngoscope. 1998;108:494–496
  32. Caraci P, Aversa S, Mussa A, Pancani G, Ondolo C, Conticello S. Role of fine-needle aspiration biopsy and frozen-section evaluation in the surgical management of thyroid nodules. Br J Surg. 2002;89:797–801
  33. Miller B, Burkey S, Lindberg G, Snyder WH, Nwariaku FE. Prevalence of malignancy within cytologically indeterminate thyroid nodules. Am J Surg. 2004;188:459–462
  34. Hamburger JI. Diagnosis of thyroid nodules by fine needle biopsy: use and abuse. J Clin Endocrinol Metab. 1994;79:335–339
  35. Hamming JF, Goslings BM, van Steenis GJ, van Ravenswaay Claasen H, Hermans J, van de Velde CJ. The value of fine-needle aspiration biopsy in patients with nodular thyroid disease divided into groups of suspicion of malignant neoplasms on clinical grounds. Arch Intern Med. 1990;150:113–116
  36. Hegedus L. Clinical practice. The thyroid nodule. N Engl J Med. 2004;351:1764–1771
  37. Asp AA, Georgitis W, Waldron EJ, Sims JE, Kidd GS. Fine needle aspiration of the thyroid. Use in an average health care facility. Am J Med. 1987;83:489–493
  38. Hanni CL, Bratt HJ, Dean RE, Vanvliet PD. Fine needle aspiration biopsy. A reliable diagnostic tool in the management of thyroid nodules. Am Surg. 1984;50:485–487
  39. Sobin LH, Wittekind C. TNM classification of malignant tumours. 5th ed.. New York: Wiley; 1997;
  40. Wittekind C, Compton CC, Greene FL, Sobin LH. TNM residual tumor classification revisited. Cancer. 2002;94:2511–2516
  41. In:  Wittekind C,  Greene FL,  Hutter RVP,  Sobin LH,  Henson DE editor. TNM supplement: a commentary on uniform use. 3rd ed.. New York: Wiley; 2003;
  42. Wittekind C, Meyer HJ, Bootz F. International union against cancer (UICC). TNM Klassifikation maligner Tumoren. 6th ed.. New York: Springer; 2002;
  43. Steurer M, Passler C, Denk DM, Schneider B, Mancusi G, Schickinger B, et al. Functional laryngeal results after thyroidectomy and extensive recurrence nerve dissection without neuromonitoring—an analysis of more than 1000 nerves at risk. Eur Surg. 2003;35:262–267
  44. Robbins KT, Medina JE, Wolfe GT, Levine PA, Sessions RB, Pruet CW. Standardizing neck dissection terminology. Official report of the Academy's Committee for Head and Neck Surgery and Oncology. Arch Otolaryngol Head Neck Surg. 1991;117:601–605
  45. Gimm O, Rath FW, Dralle H. Pattern of lymph node metastases in papillary thyroid carcinoma. Br J Surg. 1998;85:252–254
  46. Niederle B, Roka R, Brennan MF. The transplantation of parathyroid tissue in man: development, indications, technique, and results. Endocr Rev. 1982;3:245–279
  47. Sheu SY, Gorges R, Schmid KW. [Hyperplasia of the thyroid gland]. Pathologe. 2003;24:348–356
  48. Altavilla G, Pascale M, Nenci I. Fine needle aspiration cytology of thyroid gland diseases. Acta Cytol. 1990;34:251–256
  49. Gardiner GW, de Souza FM, Carydis B, Seemann C. Fine-needle aspiration biopsy of the thyroid gland: results of a five-year experience and discussion of its clinical limitations. J Otolaryngol. 1986;15:161–165
  50. Bahar G, Braslavsky D, Shpitzer T, Feinmesser R, Avidan S, Popovtzer A, et al. The cytological and clinical value of the thyroid “follicular lesion.”. Am J Otolaryngol. 2003;24:217–220
  51. DeMay RM. Follicular lesions of the thyroid. W(h)ither follicular carcinoma?. Am J Clin Pathol. 2000;114:681–683
  52. Gardner HA, Ducatman BS, Wang HH. Predictive value of fine-needle aspiration of the thyroid in the classification of follicular lesions. Cancer. 1993;71:2598–2603
  53. Kim ES, Nam-Goong IS, Gong G, Hong SJ, Kim WB, Shong YK. Postoperative findings and risk for malignancy in thyroid nodules with cytological diagnosis of the so-called “follicular neoplasm”. Korean J Intern Med. 2003;18:94–97
  54. Smith J, Cheifetz RE, Schneidereit N, Berean K, Thomson T. Can cytology accurately predict benign follicular nodules?. Am J Surg. 2005;189:592–595
  55. Tysome JR, Chandra A, Chang F, Puwanarajah P, Elliott M, Caroll P, et al. Improving prediction of malignancy of cytologically indeterminate thyroid nodules. Br J Surg. 2009;96:1400–1405
  56. McHenry CR, Huh ES, Machekano RN. Is nodule size an independent predictor of thyroid malignancy?. Surgery. 2008;144:1062–1068
  57. Sippel RS, Elaraj DM, Khanafshar E, Zarnegar R, Kebebew E, Duh QY, et al. Tumor size predicts malignant potential in Hurthle cell neoplasms of the thyroid. World J Surg. 2008;32:702–707
  58. McHenry CR, Rosen IB, Walfish PG, Bedard Y. Influence of fine-needle aspiration biopsy and frozen section examination on the management of thyroid cancer. Am J Surg. 1993;166:353–356
  59. Mittendorf EA, Khiyami A, McHenry CR. When fine-needle aspiration biopsy cannot exclude papillary thyroid cancer: a therapeutic dilemma. Arch Surg. 2006;141:961–966
  60. Paphavasit A, Thompson GB, Hay ID, Grant CS, van Heerden JA, Ilstrup DM, et al. Follicular and Hurthle cell thyroid neoplasms. Is frozen-section evaluation worthwhile?. Arch Surg. 1997;132:674–678
  61. Gharib H, Papini E, Valcavi R, Baskin HJ, Crescenzi A, Dottorini ME, et al. American Association of Clinical Endocrinologists and Associazione Medici Endocrinologi medical guidelines for clinical practice for the diagnosis and management of thyroid nodules. Endocr Pract. 2006;12:63–102
  62. Pacini F, Schlumberger M, Dralle H, Elisei R, Smit JW, Wiersinga W. European consensus for the management of patients with differentiated thyroid carcinoma of the follicular epithelium. Eur J Endocrinol. 2006;154:787–803
  63. Shaha AR. Prophylactic central compartment dissection in thyroid cancer: a new avenue of debate. Surgery. 2009;146:1224–1227
  64. Asari R, Koperek O, Scheuba C, Riss P, Kaserer K, Hoffmann M, et al. Follicular thyroid carcinoma in an iodine-replete endemic goiter region: a prospectively collected, retrospectively analyzed clinical trial. Ann Surg. 2009;249:1023–1031
  65. Pereira JA, Jimeno J, Miquel J, Iglesias M, Munné A, Sancho JJ, et al. Nodal yield, morbidity, and recurrence after central neck dissection for papillary thyroid carcinoma. Surgery. 2005;138:1095–1100
  66. Roh JL, Park JY, Park CI. Total thyroidectomy plus neck dissection in differentiated papillary thyroid carcinoma patients: pattern of nodal metastasis, morbidity, recurrence, and postoperative levels of serum parathyroid hormone. Ann Surg. 2007;245:604–610
  67. Hay ID, Hutchinson ME, Gonzalez-Losada T, McIver B, Reinalda ME, Grant CS, et al. Papillary thyroid microcarcinoma: a study of 900 cases observed in a 60-year period. Surgery. 2008;144:980–987
  68. Lim YC, Choi EC, Yoon YH, Kim EH, Koo BS. Central lymph node metastases in unilateral papillary thyroid microcarcinoma. Br J Surg. 2009;96:253–257
  69. Gemsenjager E, Heitz PU, Martina B. Selective treatment of differentiated thyroid carcinoma. World J Surg. 1997;21:546–551
  70. Lang BH, Lo CY, Chan WF, Lam KY, Wan KY. Prognostic factors in papillary and follicular thyroid carcinoma: their implications for cancer staging. Ann Surg Oncol. 2007;14:730–738
  71. Passler C, Scheuba C, Asari R, Kaczirek K, Kaserer K, Niederle B. Importance of tumour size in papillary and follicular thyroid cancer. Br J Surg. 2005;92:184–189
  72. Mazzaferri EL, Jhiang SM. Long-term impact of initial surgical and medical therapy on papillary and follicular thyroid cancer. Am J Med. 1994;97:418–428
  73. Passler C, Scheuba C, Prager G, Kaczirek K, Kaserer K, Zettinig G, et al. Prognostic factors of papillary and follicular thyroid cancer: differences in an iodine-replete endemic goiter region. Endocr Relat Cancer. 2004;11:131–139
  74. Schlumberger MJ. Papillary and follicular thyroid carcinoma. N Engl J Med 29 1998;338:297–306.
  75. Simpson WJ, McKinney SE, Carruthers JS, Gospodarowicz MK, Sutcliffe SB, Panzarella T. Papillary and follicular thyroid cancer. Prognostic factors in 1,578 patients. Am J Med. 1987;83:479–488
  76. White ML, Gauger PG, Doherty GM. Central lymph node dissection in differentiated thyroid cancer. World J Surg. 2007;31:895–904
  77. Giles Senyurek Y, Tunca F, Boztepe H, Alagol F, Terzioglu T, Tezelman S. The long term outcome of papillary thyroid carcinoma patients without primary central lymph node dissection: expected improvement of routine dissection. Surgery. 2009;146:1188–1195
  78. Monchik JM, Simon CJ, Caragacianu DL, Thomay AA, Tsai V, Cohen J, et al. Does failure to perform prophylactic level VI node dissection leave persistent disease detectable by ultrasonography in patients with low-risk papillary carcinoma of the thyroid?. Surgery. 2009;146:1182–1187
  79. Zaydfudim V, Feurer ID, Griffin MR, Phay JE. The impact of lymph node involvement on survival in patients with papillary and follicular thyroid carcinoma. Surgery. 2008;144:1070–1077
  80. Grodski S, Cornford L, Sywak M, Sidhu S, Delbridge L. Routine level VI lymph node dissection for papillary thyroid cancer: surgical technique. ANZ J Surg. 2007;77:203–208
  81. Sywak M, Cornford L, Roach P, Stalberg P, Sidhu S, Delbridge L. Routine ipsilateral level VI lymphadenectomy reduces postoperative thyroglobulin levels in papillary thyroid cancer. Surgery. 2006;140:1000–1005
  82. Grebe SK, Hay ID. Thyroid cancer nodal metastases: biologic significance and therapeutic considerations. Surg Oncol Clin N Am. 1996;5:43–63
  83. Asari R, Passler C, Kaczirek K, Scheuba C, Niederle B. Hypoparathyroidism after total thyroidectomy: a prospective study. Arch Surg. 2008;143:132–137

PII: S0039-6060(10)00042-5

doi: 10.1016/j.surg.2010.01.020

Surgery
Volume 148, Issue 3 , Pages 516-525 , September 2010