DOI QR코드

DOI QR Code

Degenerating Thyroid Nodules: Ultrasound Diagnosis, Clinical Significance, and Management

  • Jie Ren (Department of Medical Ultrasonics, The Third Affiliated Hospital of Sun Yat-Sen University) ;
  • Jung Hwan Baek (Department of Radiology and Research Institute of Radiology, University of Ulsan College of Medicine, Asan Medical Center) ;
  • Sae Rom Chung (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) ;
  • Chan Kwon Jung (Department of Hospital Pathology, College of Medicine, The Catholic University of Korea) ;
  • Jeong Hyun Lee (Department of Radiology and Research Institute of Radiology, University of Ulsan College of Medicine, Asan Medical Center)
  • Received : 2018.09.02
  • Accepted : 2019.03.11
  • Published : 2019.06.01

Abstract

Degenerating nodules (DNs), which primarily manifest as benign thyroid nodules, are one of the main causes of discordance in ultrasonography (US) and cytological assessments. Intranodular hemorrhage is one of the mechanisms contributing to discordant nodules, and an impaired blood supply may explain further DN shrinkage and infarction. The surgical specimens can be divided into acute and chronic stages based on the histological changes, which usually mimic the US features of malignant tumors. Serial US follow-up should be recommended instead of other unnecessary procedures. However, repeated fine-needle aspiration, diagnostic surgery, or core-needle biopsy may still be necessary for indeterminable or highly suspicious DNs.

Keywords

References

  1. Alexander EK, Hurwitz S, Heering JP, Benson CB, Frates MC, Doubilet PM, et al. Natural history of benign solid and cystic thyroid nodules. Ann Intern Med 2003;138:315-318 https://doi.org/10.7326/0003-4819-138-4-200302180-00010
  2. Gharib H, Papini E, Paschke R, Duick DS, Valcavi R, Hegedus L, et al.; AACE/AME/ETA Task Force on Thyroid Nodules. American Association of Clinical Endocrinologists, Associazione Medici Endocrinologi, and European Thyroid Association medical guidelines for clinical practice for the diagnosis and management of thyroid nodules. J Endocrinol Invest 2010;33(5 Suppl):1-50 https://doi.org/10.1007/BF03346587
  3. Ha EJ, Baek JH, Lee JH, Song DE, Kim JK, Shong YK, et al. Sonographically suspicious thyroid nodules with initially benign cytologic results: the role of a core needle biopsy. Thyroid 2013;23:703-708 https://doi.org/10.1089/thy.2012.0426
  4. Lee HY, Baek JH, Ha EJ, Park JW, Lee JH, Song DE, et al. Malignant-looking thyroid nodules with size reduction: core needle biopsy results. Ultrasonography 2016;35:327-334 https://doi.org/10.14366/usg.15082
  5. Ko MS, Jeong KS, Shong YK, Gong GY, Baek JH, Lee JH. Collapsing benign cystic nodules of the thyroid gland: sonographic differentiation from papillary thyroid carcinoma. AJNR Am J Neuroradiol 2012;33:124-127 https://doi.org/10.3174/ajnr.A2732
  6. Lacout A, Chevenet C, Marcy PY. Suspicious thyroid nodule management with nondiagnostic results at cytologic examination: how to diagnosis mummified benign thyroid nodules. Radiology 2015;277:303-304 https://doi.org/10.1148/radiol.2015150912
  7. Lacout A, Chevenet C, Marcy PY. Mummified thyroid syndrome. AJR Am J Roentgenol 2016;206:837-845 https://doi.org/10.2214/AJR.15.15267
  8. Kholova I. Vanishing thyroid gland tumors: infarction as consequence of FNA? Diagn Cytopathol 2016;44:568-573 https://doi.org/10.1002/dc.23479
  9. Bhatia P, Deniwar A, Mohamed HE, Sholl A, Murad F, Aslam R, et al. Vanishing tumors of thyroid: histological variations after fine needle aspiration. Gland Surg 2016;5:270-277 https://doi.org/10.21037/gs.2016.01.05
  10. Bolat F, Kayaselcuk F, Nursal TZ, Reyhan M, Bal N, Yildirim S, et al. Histopathological changes in thyroid tissue after fine needle aspiration biopsy. Pathol Res Pract 2007;203:641-645 https://doi.org/10.1016/j.prp.2007.05.004
  11. LiVolsi VA, Merino MJ. Worrisome histologic alterations following fine-needle aspiration of the thyroid (WHAFFT). Pathol Annu 1994;29(Pt 2):99-120
  12. Polyzos SA, Patsiaoura K, Zachou K. Histological alterations following thyroid fine needle biopsy: a systematic review. Diagn Cytopathol 2009;37:455-465 https://doi.org/10.1002/dc.21055
  13. Lacout A, Isaac S, Marcy PY. Micro-medullary thyroid carcinoma: a diagnosis not to be missed. Postgrad Med J 2015;91:236-237 https://doi.org/10.1136/postgradmedj-2014-133203
  14. Cochand-Priollet B, Vielh P, Royer B, Belleannee G, Collet JF, Goubin-Versini I, et al.; sous l'egide de la Societe francaise de cytologie clinique. [Thyroid cytopathology: Bethesda System 2010]. Ann Pathol 2012;32:177-183 https://doi.org/10.1016/j.annpat.2012.02.015
  15. Yeon JS, Baek JH, Lim HK, Ha EJ, Kim JK, Song DE, et al. Thyroid nodules with initially nondiagnostic cytologic results: the role of core-needle biopsy. Radiology 2013;268:274-280 https://doi.org/10.1148/radiol.13122247
  16. Screaton NJ, Berman LH, Grant JW. US-guided core-needle biopsy of the thyroid gland. Radiology 2003;226:827-832 https://doi.org/10.1148/radiol.2263012073
  17. Gharib H, Goellner JR. Fine-needle aspiration biopsy of the thyroid: an appraisal. Ann Intern Med 1993;118:282-289 https://doi.org/10.7326/0003-4819-118-4-199302150-00007
  18. Hamburger JI, Hamburger SW. Fine needle biopsy of thyroid nodules: avoiding the pitfalls. N Y State J Med 1986;86:241-249
  19. Ito Y, Amino N, Yokozawa T, Ota H, Ohshita M, Murata N, et al. Ultrasonographic evaluation of thyroid nodules in 900 patients: comparison among ultrasonographic, cytological, and histological findings. Thyroid 2007;17:1269-1276 https://doi.org/10.1089/thy.2007.0014
  20. Kwak JY, Koo H, Youk JH, Kim MJ, Moon HJ, Son EJ, et al. Value of US correlation of a thyroid nodule with initially benign cytologic results. Radiology 2010;254:292-300 https://doi.org/10.1148/radiol.2541090460
  21. Kwak JY, Kim EK, Kim HJ, Kim MJ, Son EJ, Moon HJ. How to combine ultrasound and cytological information in decision making about thyroid nodules. Eur Radiol 2009;19:1923-1931 https://doi.org/10.1007/s00330-009-1369-7
  22. Chernyavsky VS, Shanker BA, Davidov T, Crystal JS, Eng O, Ibrahim K, et al. Is one benign fine needle aspiration enough? Ann Surg Oncol 2012;19:1472-1476 https://doi.org/10.1245/s10434-011-2079-3
  23. Kuma K, Matsuzuka F, Kobayashi A, Hirai K, Morita S, Miyauchi A, et al. Outcome of long standing solitary thyroid nodules. World J Surg 1992;16:583-587; discussion 587-588 https://doi.org/10.1007/BF02067327
  24. Aulicino MR, Kaneko M, Uinger PD. Excessive endothelial cell proliferation occurring in an organizing thyroid hematoma: report of a case and review of the literature. Endocr Pathol 1995;6:153-158 https://doi.org/10.1007/BF02739878
  25. Ersoz C, Soylu L, Erkocak EU, Tetiker T, Gumurdulu D. Histologic alterations in the thyroid gland after fine-needle aspiration. Diagn Cytopathol 1997;16:230-232 https://doi.org/10.1002/(SICI)1097-0339(199703)16:3<230::AID-DC7>3.0.CO;2-J
  26. Pandit AA, Phulpagar MD. Worrisome histologic alterations following fine needle aspiration of the thyroid. Acta Cytol 2001;45:173-179 https://doi.org/10.1159/000327273
  27. Ha EJ, Baek JH, Lee JH, Lee HY, Song DE, Kim JK, et al. A focal marked hypoechogenicity within an isoechoic thyroid nodule: is it a focal malignancy or not? Acta Radiol 2015;56:814-819 https://doi.org/10.1177/0284185114539322
  28. Jung SL, Jung CK, Kim SH, Kang BJ, Ahn KJ, Kim BS, et al. Histopathologic findings related to the indeterminate or inadequate results of fine-needle aspiration biopsy and correlation with ultrasonographic findings in papillary thyroid carcinomas. Korean J Radiol 2010;11:141-148 https://doi.org/10.3348/kjr.2010.11.2.141
  29. Chung SR, Baek JH, Park HS, Choi YJ, Sung TY, Song DE, et al. Ultrasound-pathology discordant nodules on core-needle biopsy: malignancy risk and management strategy. Thyroid 2017;27:707-713 https://doi.org/10.1089/thy.2016.0462
  30. Koo JH, Shin JH, Han BK, Ko EY, Kang SS. Cystic thyroid nodules after aspiration mimicking malignancy: sonographic characteristics. J Ultrasound Med 2010;29:1415-1421 https://doi.org/10.7863/jum.2010.29.10.1415
  31. Moon HJ, Kim EK, Kwak JY. Malignancy risk stratification in thyroid nodules with benign results on cytology: combination of thyroid imaging reporting and data system and Bethesda system. Ann Surg Oncol 2014;21:1898-1903 https://doi.org/10.1245/s10434-014-3556-2
  32. Shin JH, Baek JH, Chung J, Ha EJ, Kim JH, Lee YH, et al.; Korean Society of Thyroid Radiology (KSThR) and Korean Society of Radiology. 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
  33. Kim JH, Na DG, Lee H. Ultrasonographic echogenicity and histopathologic correlation of thyroid nodules in core needle biopsy specimens. Korean J Radiol 2018;19:673-681 https://doi.org/10.3348/kjr.2018.19.4.673
  34. Papini E, Guglielmi R, Bianchini A, Crescenzi A, Taccogna S, Nardi F, et al. Risk of malignancy in nonpalpable thyroid nodules: predictive value of ultrasound and color-Doppler features. J Clin Endocrinol Metab 2002;87:1941-1946 https://doi.org/10.1210/jcem.87.5.8504
  35. Kim EK, Park CS, Chung WY, Oh KK, Kim DI, Lee JT, et al. New sonographic criteria for recommending fine-needle aspiration biopsy of nonpalpable solid nodules of the thyroid. AJR Am J Roentgenol 2002;178:687-691 https://doi.org/10.2214/ajr.178.3.1780687
  36. Frates MC, Benson CB, Doubilet PM, Cibas ES, Marqusee E. Can color Doppler sonography aid in the prediction of malignancy of thyroid nodules? J Ultrasound Med 2003;22:127-131; quiz 132-134 https://doi.org/10.7863/jum.2003.22.2.127
  37. Iannuccilli JD, Cronan JJ, Monchik JM. Risk for malignancy of thyroid nodules as assessed by sonographic criteria: the need for biopsy. J Ultrasound Med 2004;23:1455-1464 https://doi.org/10.7863/jum.2004.23.11.1455
  38. Moon WJ, Jung SL, Lee JH, Na DG, Baek JH, Lee YH, et al.; Thyroid Study Group, Korean Society of Neuro- and Head and Neck Radiology. Benign and malignant thyroid nodules: US differentiation--multicenter retrospective study. Radiology 2008;247:762-770 https://doi.org/10.1148/radiol.2473070944
  39. Silver RJ, Parangi S. Management of thyroid incidentalomas. Surg Clin North Am 2004;84:907-919 https://doi.org/10.1016/j.suc.2004.02.002
  40. Propper RA, Skolnick ML, Weinstein BJ, Dekker A. The nonspecificity of the thyroid halo sign. J Clin Ultrasound 1980;8:129-132 https://doi.org/10.1002/jcu.1870080206
  41. Sillery JC, Reading CC, Charboneau JW, Henrichsen TL, Hay ID, Mandrekar JN. Thyroid follicular carcinoma: sonographic features of 50 cases. AJR Am J Roentgenol 2010;194:44-54 https://doi.org/10.2214/AJR.09.3195
  42. Lacout A, Marcy PY. Highlights on power Doppler US of thyroid malignancy. Radiology 2010;257:586-587; author reply 587 https://doi.org/10.1148/radiol.100940
  43. Lacout A, Chevenet C, Marcy PY. Reverse mummified thyroid syndrome. AJR Am J Roentgenol 2016;207:W23
  44. Simpson KW, Albores-Saavedra J. Unusual findings in papillary thyroid microcarcinoma suggesting partial regression: a study of two cases. Ann Diagn Pathol 2007;11:97-102 https://doi.org/10.1016/j.anndiagpath.2006.03.008
  45. Hwang SH, Sung JM, Kim EK, Moon HJ, Kwak JY. Imaging-cytology correlation of thyroid nodules with initially benign cytology. Int J Endocrinol 2014;2014:491508
  46. Shin JH, Han BK, Ko K, Choe YH, Oh YL. Value of repeat ultrasound-guided fine-needle aspiration in nodules with benign cytological diagnosis. Acta Radiol 2006;47:469-473 https://doi.org/10.1080/02841850600635921
  47. Nasrollah N, Trimboli P, Guidobaldi L, Cicciarella Modica DD, Ventura C, Ramacciato G, et al. Thin core biopsy should help to discriminate thyroid nodules cytologically classified as indeterminate. A new sampling technique. Endocrine 2013;43:659-665 https://doi.org/10.1007/s12020-012-9811-z
  48. Park KT, Ahn SH, Mo JH, Park YJ, Park DJ, Choi SI, et al. Role of core needle biopsy and ultrasonographic finding in management of indeterminate thyroid nodules. Head Neck 2011;33:160-165 https://doi.org/10.1002/hed.21414
  49. Suh CH, Baek JH, Lee JH, Choi YJ, Kim JK, Sung TY, et al. The role of core-needle biopsy as a first-line diagnostic tool for initially detected thyroid nodules. Thyroid 2016;26:395-403 https://doi.org/10.1089/thy.2015.0404
  50. Yoon JH, Kim EK, Kwak JY, Moon HJ. Effectiveness and limitations of core needle biopsy in the diagnosis of thyroid nodules: review of current literature. J Pathol Transl Med 2015;49:230-235 https://doi.org/10.4132/jptm.2015.03.21
  51. Zhang M, Zhang Y, Fu S, Lv F, Tang J. Thyroid nodules with suspicious ultrasound findings: the role of ultrasound-guided core needle biopsy. Clin Imaging 2014;38:434-438 https://doi.org/10.1016/j.clinimag.2014.03.010
  52. Trimboli P, Nasrollah N, Guidobaldi L, Taccogna S, Cicciarella Modica DD, Amendola S, et al. The use of core needle biopsy as first-line in diagnosis of thyroid nodules reduces false negative and inconclusive data reported by fine-needle aspiration. World J Surg Oncol 2014;12:61