Diagnostic Performance of Ultrasound Patterns by K-TIRADS and 2015 ATA Guidelines in Risk Stratification of Thyroid Nodules and Follicular Lesions of Undetermined Significance
Hyun Sook Hong1 and Ji Ye Lee1,2
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- Affiliations:
1Department of Radiology, Soonchunhyang University, Bucheon Hospital, 170 Jomaru-ro, Wonmi-gu, Bucheon-si, Gyeonggi-do 420-767, Republic of Korea.
2Department of Radiology, Eulji Medical Center, Eulji University College of Medicine, Seoul, Republic of Korea.
Citation: American Journal of Roentgenology. 2019;213: 444-450. 10.2214/AJR.18.20961
AbstractFull TextReferencesPDFPDF PlusAdd to FavoritesPermissionsDownload Citation
ABSTRACT :
OBJECTIVE. The objective of our study was to assess the malignancy rates of thyroid nodules in the cytologically determined subclass of atypia of undetermined significance or follicular lesion of undetermined significance (AUS/FLUS) and to assess the diagnostic performance of ultrasound (US) patterns defined by the Korean Thyroid Imaging Reporting and Data System (K-TIRADS) and the 2015 American Thyroid Association (ATA) guidelines for risk stratification of AUS/FLUS nodules.
MATERIALS AND METHODS. From January 2010 to December 2016, 1340 thyroid nodules were diagnosed as AUS/FLUS via fine-needle aspiration biopsy. Of these, 683 cytopathologically confirmed nodules were included in this study. Each nodule was assigned to a category and US pattern, as defined by the K-TIRADS and ATA guidelines. US patterns were compared between benign and malignant nodules, and malignancy rates were calculated according to the subclasses of AUS/FLUS nodules and the K-TIRADS and ATA guidelines. Predictors of malignancy were assessed using logistic regression analysis.
RESULTS. The overall malignancy rate of AUS/FLUS nodules was 47.4% (324/683). There were significant differences in malignancy risk among the subclasses (p = 0.001). There were significant differences in malignancy rates according to US patterns, K-TIRADS categories, and ATA categories (p < 0.001). The malignancy rates in the K-TIRADS categories of benign, low, intermediate, and high suspicion were 0%, 1.99%, 34.66%, and 89.00%, respectively (p < 0.001). The malignancy rates in the ATA categories of benign, very low, low, intermediate, and high suspicion were 0%, 0%, 3.33%, 33.54%, and 87.67% (p < 0.001).
CONCLUSION. AUS/FLUS nodules with a final diagnosis of malignancy had significantly higher rates of suspicious US features and different K-TIRADS and ATA categories than benign nodules. US categories by K-TIRADS and ATA guidelines can be useful in predicting malignancy and risk stratification, and management planning can be adjusted according to US pattern.
Keywords: atypia of undetermined significance or follicular lesion of undetermined significance (AUS/FLUS), Bethesda System for Reporting Thyroid Cytopathology (BSRTC), sonography, thyroid nodule
Supported by the Soonchunhyang University Research Fund.
Acknowledgment
Previous sectionNext section
We thank Bora Lee (Research & Development Center, Rexsoft Co., Ltd.; Graduate School of Public Health, Seoul National University) for the statistical analysis.
References
Previous section
1. Guth S, Theune U, Aberle J, Galach A, Bamberger CM. Very high prevalence of thyroid nodules detected by high frequency (13 MHz) ultrasound examination. Eur J Clin Invest 2009; 39:699–706 [Crossref] [Medline] [Google Scholar]
2. Haugen BR, Alexander EK, Bible KC, 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 [Crossref] [Medline] [Google Scholar]
3. Yassa L, Cibas ES, Benson CB, et al. Long-term assessment of a multidisciplinary approach to thyroid nodule diagnostic evaluation. Cancer 2007; 111:508–516 [Crossref] [Medline] [Google Scholar]
4. Cibas ES, Ali SZ; NCI Thyroid FNA State of the Science Conference. The Bethesda system for reporting thyroid cytopathology. Am J Clin Pathol 2009; 132:658–665 [Crossref] [Medline] [Google Scholar]
5. Wu HH, Inman A, Cramer HM. Subclassification of “atypia of undetermined significance” in thyroid fine-needle aspirates. Diagn Cytopathol 2014; 42:23–29 [Crossref] [Medline] [Google Scholar]
6. Ho AS, Sarti EE, Jain KS, et al. Malignancy rate in thyroid nodules classified as Bethesda category III (AUS/FLUS). Thyroid 2014; 24:832–839 [Crossref] [Medline] [Google Scholar]
7. Jeong SH, Hong HS, Lee EH, Cha JG, Park JS, Kwak JJ. Outcome of thyroid nodules characterized as atypia of undetermined significance or follicular lesion of undetermined significance and correlation with ultrasound features and BRAFV600E mutation analysis. AJR 2013; 201:[web]W854–W860 [Abstract] [Google Scholar]
8. Rosario PW. Thyroid nodules with atypia or follicular lesions of undetermined significance (Bethesda category III): importance of ultrasonography and cytological subcategory. Thyroid 2014; 24:1115–1120 [Crossref] [Medline] [Google Scholar]
9. Valderrabano P, Khazai L, Thompson ZJ, et al. Cancer risk associated with nuclear atypia in cytologically indeterminate thyroid nodules: a systematic review and meta-analysis. Thyroid 2018; 28:210–219 [Crossref] [Medline] [Google Scholar]
10. Lee KH, Shin JH, Oh YL, Hahn SY. Atypia of undetermined significance in thyroid fine-needle aspiration cytology: prediction of malignancy by US and comparison of methods for further management. Ann Surg Oncol 2014; 21:2326–2331 [Crossref] [Medline] [Google Scholar]
11. Yoon JH, Kwon HJ, Kim EK, Moon HJ, Kwak JY. Subcategorization of atypia of undetermined significance/follicular lesion of undetermined significance (AUS/FLUS): a study applying Thyroid Imaging Reporting and Data System (TIRADS). Clin Endocrinol (Oxf) 2016; 85:275–282 [Crossref] [Medline] [Google Scholar]
12. Gharib H, Papini E, Garber JR, et al.; AACE/ACE/AME 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: 2016 update. Endocr Pract 2016; 22:622–639 [Crossref] [Medline] [Google Scholar]
13. Shin JH, Baek JH, Chung J, 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 [Crossref] [Medline] [Google Scholar]
14. Persichetti A, Di Stasio E, Guglielmi R, et al. Predictive value of malignancy of thyroid nodule ultrasound classification systems: a prospective study. J Clin Endocrinol Metab 2018; 103:1359–1368 [Crossref] [Medline] [Google Scholar]
15. Lauria Pantano A, Maddaloni E, Briganti SI, et al. Differences between ATA, AACE/ACE/AME and ACR TI-RADS ultrasound classifications performance in identifying cytological high-risk thyroid nodules. Eur J Endocrinol 2018; 178:595–603 [Crossref] [Medline] [Google Scholar]
16. Lee JH, Han K, Kim EK, et al. Risk stratification of thyroid nodules with atypia of undetermined significance/follicular lesion of undetermined significance (AUS/FLUS) cytology using ultrasonography patterns defined by the 2015 ATA guidelines. Ann Otol Rhinol Laryngol 2017; 126:625–633 [Crossref] [Medline] [Google Scholar]
17. Szczepanek-Parulska E, Woliński K, Stangierski A, et al. Comparison of diagnostic value of conventional ultrasonography and shear wave elastography in the prediction of thyroid lesions malignancy. PLoS One 2013; 8:e81532 [Crossref] [Medline] [Google Scholar]
18. Miller B, Burkey S, Lindberg G, Snyder WH 3rd, Nwariaku FE. Prevalence of malignancy within cytologically indeterminate thyroid nodules. Am J Surg 2004; 188:459–462 [Crossref] [Medline] [Google Scholar]
19. Banks ND, Kowalski J, Tsai HL, et al. A diagnostic predictor model for indeterminate or suspicious thyroid FNA samples. Thyroid 2008; 18:933–941 [Crossref] [Medline] [Google Scholar]
20. Sahin M, Gursoy A, Tutuncu NB, Guvener DN. Prevalence and prediction of malignancy in cytologically indeterminate thyroid nodules. Clin Endocrinol (Oxf) 2006; 65:514–518 [Crossref] [Medline] [Google Scholar]
21. Gweon HM, Son EJ, Youk JH, Kim JA. Thyroid nodules with Bethesda system III cytology: can ultrasonography guide the next step? Ann Surg Oncol 2013; 20:3083–3088 [Crossref] [Medline] [Google Scholar]
22. Broome JT, Solorzano CC. The impact of atypia/follicular lesion of undetermined significance on the rate of malignancy in thyroid fine-needle aspiration: evaluation of the Bethesda System for reporting thyroid cytopathology. Surgery 2011; 150:1234–1241 [Crossref] [Medline] [Google Scholar]
23. Olson MT, Boonyaarunnate T, Aragon Han P, Umbricht CB, Ali SZ, Zeiger MA. A tertiary center's experience with second review of 3885 thyroid cytopathology specimens. J Clin Endocrinol Metab 2013; 98:1450–1457 [Crossref] [Medline] [Google Scholar]
24. Bajaj J, Morgenstern N, Sugrue C, Wasserman J, Wasserman P. Clinical impact of second opinion in thyroid fine needle aspiration cytology (FNAC): a study of 922 interinstitutional consultations. Diagn Cytopathol 2012; 40:422–429 [Crossref] [Medline] [Google Scholar]
25. Cibas ES, Baloch ZW, Fellegara G, et al. A prospective assessment defining the limitations of thyroid nodule pathologic evaluation. Ann Intern Med 2013; 159:325–332 [Crossref] [Medline] [Google Scholar]
26. Lloyd RV, Erickson LA, Casey MB, et al. Observer variation in the diagnosis of follicular variant of papillary thyroid carcinoma. Am J Surg Pathol 2004; 28:1336–1340 [Crossref] [Medline] [Google Scholar]
27. Walts AE, Mirocha J, Bose S. Follicular lesion of undetermined significance in thyroid FNA revisited. Diagn Cytopathol 2014; 42:18–22 [Crossref] [Medline] [Google Scholar]
28. Alexander EK, Kennedy GC, Baloch ZW, et al. Preoperative diagnosis of benign thyroid nodules with indeterminate cytology. N Engl J Med 2012; 367:705–715 [Crossref] [Medline] [Google Scholar]
29. Nikiforov YE, Ohori NP, Hodak SP, et al. Impact of mutational testing on the diagnosis and management of patients with cytologically indeterminate thyroid nodules: a prospective analysis of 1056 FNA samples. J Clin Endocrinol Metab 2011; 96:3390–3397 [Crossref] [Medline] [Google Scholar]
Address correspondence to H. S. Hong (hshong@schmc.ac.kr).
Read More: https://www.ajronline.org/doi/abs/10.2214/AJR.18.20961
Hyun Sook Hong1 and Ji Ye Lee1,2
Share Share
- Affiliations:
1Department of Radiology, Soonchunhyang University, Bucheon Hospital, 170 Jomaru-ro, Wonmi-gu, Bucheon-si, Gyeonggi-do 420-767, Republic of Korea.
2Department of Radiology, Eulji Medical Center, Eulji University College of Medicine, Seoul, Republic of Korea.
Citation: American Journal of Roentgenology. 2019;213: 444-450. 10.2214/AJR.18.20961
AbstractFull TextReferencesPDFPDF PlusAdd to FavoritesPermissionsDownload Citation
ABSTRACT :
OBJECTIVE. The objective of our study was to assess the malignancy rates of thyroid nodules in the cytologically determined subclass of atypia of undetermined significance or follicular lesion of undetermined significance (AUS/FLUS) and to assess the diagnostic performance of ultrasound (US) patterns defined by the Korean Thyroid Imaging Reporting and Data System (K-TIRADS) and the 2015 American Thyroid Association (ATA) guidelines for risk stratification of AUS/FLUS nodules.
MATERIALS AND METHODS. From January 2010 to December 2016, 1340 thyroid nodules were diagnosed as AUS/FLUS via fine-needle aspiration biopsy. Of these, 683 cytopathologically confirmed nodules were included in this study. Each nodule was assigned to a category and US pattern, as defined by the K-TIRADS and ATA guidelines. US patterns were compared between benign and malignant nodules, and malignancy rates were calculated according to the subclasses of AUS/FLUS nodules and the K-TIRADS and ATA guidelines. Predictors of malignancy were assessed using logistic regression analysis.
RESULTS. The overall malignancy rate of AUS/FLUS nodules was 47.4% (324/683). There were significant differences in malignancy risk among the subclasses (p = 0.001). There were significant differences in malignancy rates according to US patterns, K-TIRADS categories, and ATA categories (p < 0.001). The malignancy rates in the K-TIRADS categories of benign, low, intermediate, and high suspicion were 0%, 1.99%, 34.66%, and 89.00%, respectively (p < 0.001). The malignancy rates in the ATA categories of benign, very low, low, intermediate, and high suspicion were 0%, 0%, 3.33%, 33.54%, and 87.67% (p < 0.001).
CONCLUSION. AUS/FLUS nodules with a final diagnosis of malignancy had significantly higher rates of suspicious US features and different K-TIRADS and ATA categories than benign nodules. US categories by K-TIRADS and ATA guidelines can be useful in predicting malignancy and risk stratification, and management planning can be adjusted according to US pattern.
Keywords: atypia of undetermined significance or follicular lesion of undetermined significance (AUS/FLUS), Bethesda System for Reporting Thyroid Cytopathology (BSRTC), sonography, thyroid nodule
Supported by the Soonchunhyang University Research Fund.
Acknowledgment
Previous sectionNext section
We thank Bora Lee (Research & Development Center, Rexsoft Co., Ltd.; Graduate School of Public Health, Seoul National University) for the statistical analysis.
References
Previous section
1. Guth S, Theune U, Aberle J, Galach A, Bamberger CM. Very high prevalence of thyroid nodules detected by high frequency (13 MHz) ultrasound examination. Eur J Clin Invest 2009; 39:699–706 [Crossref] [Medline] [Google Scholar]
2. Haugen BR, Alexander EK, Bible KC, 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 [Crossref] [Medline] [Google Scholar]
3. Yassa L, Cibas ES, Benson CB, et al. Long-term assessment of a multidisciplinary approach to thyroid nodule diagnostic evaluation. Cancer 2007; 111:508–516 [Crossref] [Medline] [Google Scholar]
4. Cibas ES, Ali SZ; NCI Thyroid FNA State of the Science Conference. The Bethesda system for reporting thyroid cytopathology. Am J Clin Pathol 2009; 132:658–665 [Crossref] [Medline] [Google Scholar]
5. Wu HH, Inman A, Cramer HM. Subclassification of “atypia of undetermined significance” in thyroid fine-needle aspirates. Diagn Cytopathol 2014; 42:23–29 [Crossref] [Medline] [Google Scholar]
6. Ho AS, Sarti EE, Jain KS, et al. Malignancy rate in thyroid nodules classified as Bethesda category III (AUS/FLUS). Thyroid 2014; 24:832–839 [Crossref] [Medline] [Google Scholar]
7. Jeong SH, Hong HS, Lee EH, Cha JG, Park JS, Kwak JJ. Outcome of thyroid nodules characterized as atypia of undetermined significance or follicular lesion of undetermined significance and correlation with ultrasound features and BRAFV600E mutation analysis. AJR 2013; 201:[web]W854–W860 [Abstract] [Google Scholar]
8. Rosario PW. Thyroid nodules with atypia or follicular lesions of undetermined significance (Bethesda category III): importance of ultrasonography and cytological subcategory. Thyroid 2014; 24:1115–1120 [Crossref] [Medline] [Google Scholar]
9. Valderrabano P, Khazai L, Thompson ZJ, et al. Cancer risk associated with nuclear atypia in cytologically indeterminate thyroid nodules: a systematic review and meta-analysis. Thyroid 2018; 28:210–219 [Crossref] [Medline] [Google Scholar]
10. Lee KH, Shin JH, Oh YL, Hahn SY. Atypia of undetermined significance in thyroid fine-needle aspiration cytology: prediction of malignancy by US and comparison of methods for further management. Ann Surg Oncol 2014; 21:2326–2331 [Crossref] [Medline] [Google Scholar]
11. Yoon JH, Kwon HJ, Kim EK, Moon HJ, Kwak JY. Subcategorization of atypia of undetermined significance/follicular lesion of undetermined significance (AUS/FLUS): a study applying Thyroid Imaging Reporting and Data System (TIRADS). Clin Endocrinol (Oxf) 2016; 85:275–282 [Crossref] [Medline] [Google Scholar]
12. Gharib H, Papini E, Garber JR, et al.; AACE/ACE/AME 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: 2016 update. Endocr Pract 2016; 22:622–639 [Crossref] [Medline] [Google Scholar]
13. Shin JH, Baek JH, Chung J, 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 [Crossref] [Medline] [Google Scholar]
14. Persichetti A, Di Stasio E, Guglielmi R, et al. Predictive value of malignancy of thyroid nodule ultrasound classification systems: a prospective study. J Clin Endocrinol Metab 2018; 103:1359–1368 [Crossref] [Medline] [Google Scholar]
15. Lauria Pantano A, Maddaloni E, Briganti SI, et al. Differences between ATA, AACE/ACE/AME and ACR TI-RADS ultrasound classifications performance in identifying cytological high-risk thyroid nodules. Eur J Endocrinol 2018; 178:595–603 [Crossref] [Medline] [Google Scholar]
16. Lee JH, Han K, Kim EK, et al. Risk stratification of thyroid nodules with atypia of undetermined significance/follicular lesion of undetermined significance (AUS/FLUS) cytology using ultrasonography patterns defined by the 2015 ATA guidelines. Ann Otol Rhinol Laryngol 2017; 126:625–633 [Crossref] [Medline] [Google Scholar]
17. Szczepanek-Parulska E, Woliński K, Stangierski A, et al. Comparison of diagnostic value of conventional ultrasonography and shear wave elastography in the prediction of thyroid lesions malignancy. PLoS One 2013; 8:e81532 [Crossref] [Medline] [Google Scholar]
18. Miller B, Burkey S, Lindberg G, Snyder WH 3rd, Nwariaku FE. Prevalence of malignancy within cytologically indeterminate thyroid nodules. Am J Surg 2004; 188:459–462 [Crossref] [Medline] [Google Scholar]
19. Banks ND, Kowalski J, Tsai HL, et al. A diagnostic predictor model for indeterminate or suspicious thyroid FNA samples. Thyroid 2008; 18:933–941 [Crossref] [Medline] [Google Scholar]
20. Sahin M, Gursoy A, Tutuncu NB, Guvener DN. Prevalence and prediction of malignancy in cytologically indeterminate thyroid nodules. Clin Endocrinol (Oxf) 2006; 65:514–518 [Crossref] [Medline] [Google Scholar]
21. Gweon HM, Son EJ, Youk JH, Kim JA. Thyroid nodules with Bethesda system III cytology: can ultrasonography guide the next step? Ann Surg Oncol 2013; 20:3083–3088 [Crossref] [Medline] [Google Scholar]
22. Broome JT, Solorzano CC. The impact of atypia/follicular lesion of undetermined significance on the rate of malignancy in thyroid fine-needle aspiration: evaluation of the Bethesda System for reporting thyroid cytopathology. Surgery 2011; 150:1234–1241 [Crossref] [Medline] [Google Scholar]
23. Olson MT, Boonyaarunnate T, Aragon Han P, Umbricht CB, Ali SZ, Zeiger MA. A tertiary center's experience with second review of 3885 thyroid cytopathology specimens. J Clin Endocrinol Metab 2013; 98:1450–1457 [Crossref] [Medline] [Google Scholar]
24. Bajaj J, Morgenstern N, Sugrue C, Wasserman J, Wasserman P. Clinical impact of second opinion in thyroid fine needle aspiration cytology (FNAC): a study of 922 interinstitutional consultations. Diagn Cytopathol 2012; 40:422–429 [Crossref] [Medline] [Google Scholar]
25. Cibas ES, Baloch ZW, Fellegara G, et al. A prospective assessment defining the limitations of thyroid nodule pathologic evaluation. Ann Intern Med 2013; 159:325–332 [Crossref] [Medline] [Google Scholar]
26. Lloyd RV, Erickson LA, Casey MB, et al. Observer variation in the diagnosis of follicular variant of papillary thyroid carcinoma. Am J Surg Pathol 2004; 28:1336–1340 [Crossref] [Medline] [Google Scholar]
27. Walts AE, Mirocha J, Bose S. Follicular lesion of undetermined significance in thyroid FNA revisited. Diagn Cytopathol 2014; 42:18–22 [Crossref] [Medline] [Google Scholar]
28. Alexander EK, Kennedy GC, Baloch ZW, et al. Preoperative diagnosis of benign thyroid nodules with indeterminate cytology. N Engl J Med 2012; 367:705–715 [Crossref] [Medline] [Google Scholar]
29. Nikiforov YE, Ohori NP, Hodak SP, et al. Impact of mutational testing on the diagnosis and management of patients with cytologically indeterminate thyroid nodules: a prospective analysis of 1056 FNA samples. J Clin Endocrinol Metab 2011; 96:3390–3397 [Crossref] [Medline] [Google Scholar]
Address correspondence to H. S. Hong (hshong@schmc.ac.kr).
Read More: https://www.ajronline.org/doi/abs/10.2214/AJR.18.20961
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