Korean Journal of Radiology

The Korean Society of Radiology (대한영상의학회)
권호 표지
DOI QR코드

DOI QR Code

Sonographic Diagnosis of Cervical Lymph Node Metastasis in Patients with Thyroid Cancer and Comparison of European and Korean Guidelines for Stratifying the Risk of Malignant Lymph Node

  • Sae Rom Chung (Department of Radiology and Research Institute of Radiology, University of Ulsan College of Medicine, Asan Medical Center) ;
  • Jung Hwan Baek (Department of Radiology and Research Institute of Radiology, University of Ulsan College of Medicine, Asan Medical Center) ;
  • Yun Hwa Rho (Department of Radiology and Research Institute of Radiology, University of Ulsan College of Medicine, Asan Medical Center) ;
  • Young Jun Choi (Department of Radiology and Research Institute of Radiology, University of Ulsan College of Medicine, Asan Medical Center) ;
  • Tae-Yon Sung (Department of Surgery, University of Ulsan College of Medicine, Asan Medical Center) ;
  • Dong Eun Song (Department of Pathology, University of Ulsan College of Medicine, Asan Medical Center) ;
  • Tae Yong Kim (Department of Internal Medicine, University of Ulsan College of Medicine, Asan Medical Center) ;
  • Jeong Hyun Lee (Department of Radiology and Research Institute of Radiology, University of Ulsan College of Medicine, Asan Medical Center)
  • Received : 2021.04.16
  • Accepted : 2022.08.18
  • Published : 2022.11.01
Download PDF
⟨ Previous Next ⟩

Abstract

Objective: To evaluate the ultrasonography (US) features for diagnosing metastasis in cervical lymph nodes (LNs) in patients with thyroid cancer and compare the US classification of risk of LN metastasis between European and Korean guidelines. Materials and Methods: From January 2014 to December 2018, US-guided fine-needle aspiration was performed on 836 LNs from 714 patients for the preoperative nodal staging of thyroid cancer. The US features of LNs were retrospectively reviewed for the following features: size, presence of hilum, margin, orientation, cystic change, punctate echogenic foci (PEF), large echogenic foci, eccentric cortical thickening, abnormal vascularity, and cortical hyperechogenicity. A multiple logistic regression analysis was performed to identify the independent US features for the diagnosis of metastatic LNs. The diagnostic performance of independent US features was subsequently evaluated. LNs were categorized according to the Korean Thyroid Imaging Reporting and Data System (K-TIRADS) and European Thyroid Association (ETA) guidelines, and the correlation between the two sets of classifications was assessed. Results: Absence of the hilum, presence of cystic changes, PEF, abnormal vascularity, and cortical hyperechogenicity were independent US features of metastatic LNs. Cystic changes, PEF, abnormal vascularity, and cortical hyperechogenicity showed high specificity (86.8%-99.6%). The absence of the hilum had the highest sensitivity yet low specificity (66.4%). When LNs were classified according to the ETA guidelines and K-TIRADS, they yielded similar categorizations of malignancy risks and were strongly correlated (Spearman coefficient, 0.9766 [95% confidence interval, 0.973-0.979]). According to the ETA guidelines, 9.8% (82/836) of LNs were classified as "not specified." Conclusion: Absence of hilum, cystic changes, PEF, abnormal vascularity, and cortical hyperechogenicity were independent US features suggestive of metastatic LNs in thyroid cancer. Both K-TIRADS and the ETA guidelines provided similar risk stratification for metastatic LNs with a high correlation; however, the ETA guidelines failed to classify 9.8% of LNs into a specific risk stratum. These results may provide a basis for revising LN classification in future guidelines.

Keywords

References

  1. Arianpoor A, Asadi M, Amini E, Ziaeemehr A, Ahmadi Simab S, Zakavi SR. Investigating the prevalence of risk factors of papillary thyroid carcinoma recurrence and disease-free survival after thyroidectomy and central neck dissection in Iranian patients. Acta Chir Belg 2020;120:173-178
  2. King JM, Corbitt C, Miller FR. Management of lateral cervical metastases in papillary thyroid cancer: patterns of lymph node distribution. Ear Nose Throat J 2011;90:386-389
  3. Shaha AR. Management of the neck in thyroid cancer. Otolaryngol Clin North Am 1998;31:823-831
  4. Roh JL, Kim JM, Park CI. Lateral cervical lymph node metastases from papillary thyroid carcinoma: pattern of nodal metastases and optimal strategy for neck dissection. Ann Surg Oncol 2008;15:1177-1182
  5. McGregor GI, Luoma A, Jackson SM. Lymph node metastases from well-differentiated thyroid cancer. A clinical review. Am J Surg 1985;149:610-612
  6. Watkinson JC, Franklyn JA, Olliff JF. Detection and surgical treatment of cervical lymph nodes in differentiated thyroid cancer. Thyroid 2006;16:187-194
  7. Ito Y, Kudo T, Kobayashi K, Miya A, Ichihara K, Miyauchi A. Prognostic factors for recurrence of papillary thyroid carcinoma in the lymph nodes, lung, and bone: analysis of 5,768 patients with average 10-year follow-up. World J Surg 2012;36:1274-1278
  8. Ywata de Carvalho A, Kohler HF, Gomes CC, Vartanian JG, Kowalski LP. Predictive factors for recurrence of papillary thyroid carcinoma: analysis of 4,085 patients. Acta Otorhinolaryngol Ital 2021;41:236-242
  9. 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
  10. 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
  11. Jeon SJ, Kim E, Park JS, Son KR, Baek JH, Kim YS, et al. Diagnostic benefit of thyroglobulin measurement in fine-needle aspiration for diagnosing metastatic cervical lymph nodes from papillary thyroid cancer: correlations with US features. Korean J Radiol 2009;10:106-111
  12. Miseikyte-Kaubriene E, Trakymas M, Ulys A. Cystic lymph node metastasis in papillary thyroid carcinoma. Medicina (Kaunas) 2008;44:455-459
  13. 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
  14. Kessler A, Rappaport Y, Blank A, Marmor S, Weiss J, Graif M. Cystic appearance of cervical lymph nodes is characteristic of metastatic papillary thyroid carcinoma. J Clin Ultrasound 2003;31:21-25
  15. Wunderbaldinger P, Harisinghani MG, Hahn PF, Daniels GH, Turetschek K, Simeone J, et al. Cystic lymph node metastases in papillary thyroid carcinoma. AJR Am J Roentgenol 2002;178:693-697
  16. 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
  17. 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
  18. Ha EJ, Chung SR, Na DG, Ahn HS, Chung J, Lee JY, et al. 2021 Korean thyroid imaging reporting and data system and imaging-based management of thyroid nodules: Korean Society of Thyroid Radiology consensus statement and recommendations. Korean J Radiol 2021;22:2094-2123
  19. 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
  20. Kim DW, Choo HJ, Lee YJ, Jung SJ, Eom JW, Ha TK. Sonographic features of cervical lymph nodes after thyroidectomy for papillary thyroid carcinoma. J Ultrasound Med 2013;32:1173-1180
  21. Yoo YH, Kim JA, Son EJ, Youk JH, Kwak JY, Kim EK, et al. Sonographic findings predictive of central lymph node metastasis in patients with papillary thyroid carcinoma: influence of associated chronic lymphocytic thyroiditis on the diagnostic performance of sonography. J Ultrasound Med 2013;32:2145-2151
  22. 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
  23. Cohen JF, Korevaar DA, Altman DG, Bruns DE, Gatsonis CA, Hooft L, et al. STARD 2015 guidelines for reporting diagnostic accuracy studies: explanation and elaboration. BMJ Open 2016;6:e012799
  24. 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
  25. 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
  26. Chung SR, Baek JH, Choi YJ, Sung TY, Song DE, Kim TY, et al. Diagnostic algorithm for metastatic lymph nodes of differentiated thyroid carcinoma. Cancers (Basel) 2021;13:1338
  27. Lee JY, Yoo RE, Rhim JH, Lee KH, Choi KS, Hwang I, et al. Validation of ultrasound risk stratification systems for cervical lymph node metastasis in patients with thyroid cancer. Cancers (Basel) 2022;14:2106
  28. Marchiori E, Hochhegger B, Zanetti G. Lymph node calcifications. J Bras Pneumol 2018;44:83
  29. Eisenkraft BL, Som PM. The spectrum of benign and malignant etiologies of cervical node calcification. AJR Am J Roentgenol 1999;172:1433-1437