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Ultrasonographic Indeterminate Lymph Nodes in Preoperative Thyroid Cancer Patients: Malignancy Risk and Ultrasonographic Findings Predictive of Malignancy

  • Roh-Eul Yoo (Department of Radiology, Seoul National University Hospital) ;
  • Ji-hoon Kim (Department of Radiology, Seoul National University Hospital) ;
  • Jeong Mo Bae (Department of Pathology, Seoul National University Hospital) ;
  • Inpyeong Hwang (Department of Radiology, Seoul National University Hospital) ;
  • Koung Mi Kang (Department of Radiology, Seoul National University Hospital) ;
  • Tae Jin Yun (Department of Radiology, Seoul National University Hospital) ;
  • Seung Hong Choi (Department of Radiology, Seoul National University Hospital) ;
  • Chul-Ho Sohn (Department of Radiology, Seoul National University Hospital) ;
  • Jung Hyo Rhim (Department of Radiology, Seoul Metropolitan Government Seoul National University Boramae Medical Center) ;
  • Sun-Won Park (Department of Radiology, Seoul National University College of Medicine)
  • Received : 2019.10.10
  • Accepted : 2020.01.05
  • Published : 2020.05.01

Abstract

Objective: Proper management of lymph nodes (LNs) with ultrasonographic (US) indeterminate features in thyroid cancer patients remains elusive. We aimed to evaluate the malignancy risk and US findings predictive of malignancy for US indeterminate LNs in preoperative thyroid cancer patients through node-by-node correlation. Materials and Methods: A total of 348 LNs in 284 thyroid cancer patients, who underwent fine-needle aspiration or core-needle biopsy between December 2006 and June 2015, were included. We determined the malignancy risks for US probably benign, indeterminate, and suspicious categories. For US indeterminate LNs, which had neither echogenic hilum nor hilar vascularity in the absence of any suspicious finding, US findings were compared between benign and metastatic LNs using Mann-Whitney U test and Fisher's exact test. Results: US imaging diagnoses were probably benign in 20.7% (n = 72) cases, indeterminate in 23.6% (n = 82), and suspicious in 55.7% (n = 194). Malignancy risk of US indeterminate LNs (19.5% [16/82]) differed from those of the US probably benign (2.8% [2/72]) (p = 0.002) and US suspicious LNs (78.4% [152/194]) (p < 0.001). Among US indeterminate LNs, there were no significant differences in short, long, and long-to-short diameter (L/S) ratios between benign and metastatic LNs (3.9 vs. 3.8 mm, p = 0.619; 7.3 vs. 7.3 mm, p = 0.590; 1.9 vs. 1.9, p = 0.652). Conclusion: US indeterminate LNs were frequently encountered during preoperative evaluation and had intermediate malignancy risk. Given the lack of discriminative power of size criteria and L/S ratio, clinical factors such as surgical strategy and node size should be considered for proper triage of US indeterminate LNs in thyroid cancer.

Keywords

Acknowledgement

This study was supported by grant no. 05-2015-0050 from the SNUH Research Fund.

References

  1. Al-Saif O, Farrar WB, Bloomston M, Porter K, Ringel MD, Kloos RT. Long-term efficacy of lymph node reoperation for persistent papillary thyroid cancer. J Clin Endocrinol Metab 2010;95:2187-2194  https://doi.org/10.1210/jc.2010-0063
  2. Mazzaferri EL, Kloos RT. Clinical review 128: current approaches to primary therapy for papillary and follicular thyroid cancer. J Clin Endocrinol Metab 2001;86:1447-1463  https://doi.org/10.1210/jcem.86.4.7407
  3. Grebe SK, Hay ID. Thyroid cancer nodal metastases: biologic significance and therapeutic considerations. Surg Oncol Clin N Am 1996;5:43-63  https://doi.org/10.1016/S1055-3207(18)30404-6
  4. Scheumann GF, Gimm O, Wegener G, Hundeshagen H, Dralle H. Prognostic significance and surgical management of locoregional lymph node metastases in papillary thyroid cancer. World J Surg 1994;18:559-567;discussion 567-568  https://doi.org/10.1007/BF00353765
  5. Shah MD, Hall FT, Eski SJ, Witterick IJ, Walfish PG, Freeman JL. Clinical course of thyroid carcinoma after neck dissection. Laryngoscope 2003;113:2102-2107  https://doi.org/10.1097/00005537-200312000-00008
  6. Fish SA, Langer JE, Mandel SJ. Sonographic imaging of thyroid nodules and cervical lymph nodes. Endocrinol Metab Clin North Am 2008;37:401-417, ix  https://doi.org/10.1016/j.ecl.2007.12.003
  7. Kuna SK, Bracic I, Tesic V, Kuna K, Herceg GH, Dodig D. Ultrasonographic differentiation of benign from malignant neck lymphadenopathy in thyroid cancer. J Ultrasound Med 2006;25:1531-1537;quiz 1538-1540  https://doi.org/10.7863/jum.2006.25.12.1531
  8. Rosario PW, de Faria S, Bicalho L, Alves MF, Borges MA, Purisch S, et al. Ultrasonographic differentiation between metastatic and benign lymph nodes in patients with papillary thyroid carcinoma. J Ultrasound Med 2005;24:1385-1389  https://doi.org/10.7863/jum.2005.24.10.1385
  9. Sohn YM, Kwak JY, Kim EK, Moon HJ, Kim SJ, Kim MJ. Diagnostic approach for evaluation of lymph node metastasis from thyroid cancer using ultrasound and fine-needle aspiration biopsy. AJR Am J Roentgenol 2010;194:38-43  https://doi.org/10.2214/AJR.09.3128
  10. Haugen BR, Alexander EK, Bible KC, Doherty GM, Mandel SJ, Nikiforov YE, et al. 2015 American Thyroid Association management guidelines for adult patients with thyroid nodules and differentiated thyroid cancer: the American Thyroid Association guidelines task force on thyroid nodules and differentiated thyroid cancer. Thyroid 2016;26:1-133  https://doi.org/10.1089/thy.2015.0020
  11. Kim E, Park JS, Son KR, Kim JH, Jeon SJ, Na DG. Preoperative diagnosis of cervical metastatic lymph nodes in papillary thyroid carcinoma: comparison of ultrasound, computed tomography, and combined ultrasound with computed tomography. Thyroid 2008;18:411-418  https://doi.org/10.1089/thy.2007.0269
  12. Tessler FN, Middleton WD, Grant EG, Hoang JK, Berland LL, Teefey SA, et al. ACR thyroid imaging, reporting and data system (TI-RADS): white paper of the ACR TI-RADS committee. J Am Coll Radiol 2017;14:587-595  https://doi.org/10.1016/j.jacr.2017.01.046
  13. Lee Y, Kim JH, Baek JH, Jung SL, Park SW, Kim J, et al. Value of CT added to ultrasonography for the diagnosis of lymph node metastasis in patients with thyroid cancer. Head Neck 2018;40:2137-2148  https://doi.org/10.1002/hed.25202
  14. Leenhardt L, Erdogan MF, Hegedus L, Mandel SJ, Paschke R, Rago T, et al. 2013 European Thyroid Association guidelines for cervical ultrasound scan and ultrasound-guided techniques in the postoperative management of patients with thyroid cancer. Eur Thyroid J 2013;2:147-159  https://doi.org/10.1159/000354537
  15. Shin JH, Baek JH, Chung J, Ha EJ, Kim JH, Lee YH, et al. Ultrasonography diagnosis and imaging-based management of thyroid nodules: revised Korean Society of Thyroid Radiology consensus statement and recommendations. Korean J Radiol 2016;17:370-395  https://doi.org/10.3348/kjr.2016.17.3.370
  16. Stack BC Jr, Ferris RL, Goldenberg D, Haymart M, Shaha A, Sheth S, 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  https://doi.org/10.1089/thy.2011.0312
  17. American Thyroid Association Surgery Working Group, American Association of Endocrine Surgeons, American Academy of Otolaryngology-Head and Neck Surgery, American Head and Neck Society; Carty SE, Cooper DS, Doherty GM, Duh QY, Kloos RT, Mandel SJ, et al. Consensus statement on the terminology and classification of central neck dissection for thyroid cancer. Thyroid 2009;19:1153-1158  https://doi.org/10.1089/thy.2009.0159
  18. Landis JR, Koch GG. The measurement of observer agreement for categorical data. Biometrics 1977;33:159-174  https://doi.org/10.2307/2529310
  19. Hwang HS, Orloff LA. Efficacy of preoperative neck ultrasound in the detection of cervical lymph node metastasis from thyroid cancer. Laryngoscope 2011;121:487-491  https://doi.org/10.1002/lary.21227
  20. Sipos JA. Advances in ultrasound for the diagnosis and management of thyroid cancer. Thyroid 2009;19:1363-1372  https://doi.org/10.1089/thy.2009.1608
  21. Leboulleux S, Girard E, Rose M, Travagli JP, Sabbah N, Caillou B, et al. Ultrasound criteria of malignancy for cervical lymph nodes in patients followed up for differentiated thyroid cancer. J Clin Endocrinol Metab 2007;92:3590-3594  https://doi.org/10.1210/jc.2007-0444
  22. Ahuja A, Ying M, Evans R, King W, Metreweli C. The application of ultrasound criteria for malignancy in differentiating tuberculous cervical adenitis from metastatic nasopharyngeal carcinoma. Clin Radiol 1995;50:391-395  https://doi.org/10.1016/S0009-9260(05)83136-8
  23. Steinkamp HJ, Cornehl M, Hosten N, Pegios W, Vogl T, Felix R. Cervical lymphadenopathy: ratio of long- to short-axis diameter as a predictor of malignancy. Br J Radiol 1995;68:266-270  https://doi.org/10.1259/0007-1285-68-807-266
  24. Vassallo P, Wernecke K, Roos N, Peters PE. Differentiation of benign from malignant superficial lymphadenopathy: the role of high-resolution US. Radiology 1992;183:215-220 https://doi.org/10.1148/radiology.183.1.1549675