The Added Value of Operator's Judgement in Thyroid Nodule Ultrasound Classification Arising From Histologically Based Comparison of Different Risk Stratification Systems

Bruno Madeo, Giulia Brigante, Anna Ansaloni, Erica Taliani, Shaniko Kaleci, Maria Laura Monzani, Manuela Simoni, Vincenzo Rochira, Bruno Madeo, Giulia Brigante, Anna Ansaloni, Erica Taliani, Shaniko Kaleci, Maria Laura Monzani, Manuela Simoni, Vincenzo Rochira

Abstract

Objective: Several ultrasound classifications for thyroid nodules were proposed but their accuracy is still debated, since mainly estimated on cytology and not on histology. The aim of this study was to test the diagnostic accuracy and the inter-classification agreement of AACE/ACE-AME, American Thyroid Association (ATA), British Thyroid Association (BTA), and Modena Ultrasound Thyroid Classification (MUT) that stratifies malignancy risk considering also the clinician subjective impression. Methods: A prospective study collecting thyroid nodule features at ultrasound and histological diagnosis was conducted. Ultrasound features were collected following a preformed checklist in candidates for surgery because of indeterminate, suspicious, or malignant cytology. All the nodules, besides the cytologically suspicious one, were blinded analyzed. MUT score was applied prospectively, and the others retrospectively. Sensitivity, specificity, diagnostic cut-off value, and accuracy of each classification were calculated. The overall agreement between classifications was tested by Bland-Altman, and agreement between single nodule analysis by different classifications by Weighted Cohen's Kappa. Results: In classifying a total of 457 nodules, MUT has the highest accuracy (AUC 0.808) and specificity (89%), followed by ATA and BTA, and finally by AACE/ACE-AME. ATA, BTA, and MUT are highly interchangeable. Considering agreement between single nodule analyses, ATA and BTA had the best (κ = 0.723); AACE/ACE-AME showed slight agreement with BTA (κ = 0.177) and MUT (κ = 0.183), and fair agreement with ATA (κ = 0.282); MUT had fair agreement with both ATA (κ = 0.291) and BTA (κ = 0.271). Conclusion: Classifications have an acceptable overall diagnostic accuracy, improved using a less rigid system that takes into consideration operator subjective impression.

Keywords: classifications; histology; malignancy risk; thyroid nodules; ultrasound.

Copyright © 2020 Madeo, Brigante, Ansaloni, Taliani, Kaleci, Monzani, Simoni and Rochira.

Figures

Figure 1
Figure 1
Preformed checklist used for the collection of nodules features during ultrasound examination.
Figure 2
Figure 2
Nodules distribution according to AACE/ACE-AME Task Force on thyroid nodules, American Thyroid Association (ATA), British Thyroid Association (BTA), and Modena US Thyroid Classification (MUT). Benignity and malignancy have been diagnosed histologically according to histology. Numbers in bars are expressed as percentage of the total number of nodules for each category.
Figure 3
Figure 3
ROC curve that describes the relationship between the sensitivity and specificity of the four classification systems [AACE/ACE-AME Task Force on thyroid nodules, American Thyroid Association (ATA), British Thyroid Association (BTA), and Modena US Thyroid Classification (MUT)].
Figure 4
Figure 4
Bland–Altman plots showing the differences between measurements of the classification systems. The blue line is the average of the differences (in case the first and second measurements were coincidentally, points would be aligned along the axis of the abscissas and positioned on the value 0); the dot lines are the 95% limits of agreement. (A) MUT vs. AACE/ACE-AME; (B) MUT vs. ATA; (C) MUT vs. BTA; (D) AACE/ACE-AME vs. ATA; (E) AACE/ACE-AME vs. BTA; (F) ATA vs. BTA [AACE/ACE-AME Task Force on thyroid nodules, American Thyroid Association (ATA), British Thyroid Association (BTA), and Modena US Thyroid Classification (MUT)].

References

    1. Remonti LR, Kramer CK, Leitao CB, Pinto LC, Gross JL. Thyroid ultrasound features and risk of carcinoma: a systematic review and meta-analysis of observational studies. Thyroid. (2015) 25:538–50. 10.1089/thy.2014.0353
    1. Campanella P, Ianni F, Rota CA, Corsello SM, Pontecorvi A. Quantification of cancer risk of each clinical and ultrasonographic suspicious feature of thyroid nodules: a systematic review and meta-analysis. Eur J Endocrinol. (2014) 170:R203–11. 10.1530/EJE-13-0995
    1. Brito JP, Gionfriddo MR, Al Nofal A, Boehmer KR, Leppin AL, Reading C, et al. . The accuracy of thyroid nodule ultrasound to predict thyroid cancer: systematic review and meta-analysis. J Clin Endocrinol Metab. (2014) 99:1253–63. 10.1210/jc.2013-2928
    1. Reading CC, Charboneau JW, Hay ID, Sebo TJ. Sonography of thyroid nodules: a “classic pattern” diagnostic approach. Ultrasound Q. (2005) 21:157–65. 10.1097/01.ruq.0000174750.27010.68
    1. Horvath E, Majlis S, Rossi R, Franco C, Niedmann JP, Castro A, et al. . An ultrasonogram reporting system for thyroid nodules stratifying cancer risk for clinical management. J Clin Endocrinol Metab. (2009) 94:1748–51. 10.1210/jc.2008-1724
    1. Park JY, Lee HJ, Jang HW, Kim HK, Yi JH, Lee W, et al. . A proposal for a thyroid imaging reporting and data system for ultrasound features of thyroid carcinoma. Thyroid. (2009) 19:1257–64. 10.1089/thy.2008.0021
    1. Kwak JY, Han KH, Yoon JH, Moon HJ, Son EJ, Park SH, et al. . Thyroid imaging reporting and data system for US features of nodules: a step in establishing better stratification of cancer risk. Radiology. (2011) 260:892–9. 10.1148/radiol.11110206
    1. Lee YH, Kim DW, In HS, Park JS, Kim SH, Eom JW, et al. . Differentiation between benign and malignant solid thyroid nodules using an US classification system. Korean J Radiol. (2011) 12:559–67. 10.3348/kjr.2011.12.5.559
    1. 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) 17:370–95. 10.3348/kjr.2016.17.3.370
    1. 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) 14:587–95. 10.1016/j.jacr.2017.01.046
    1. Wemeau JL, Sadoul JL, d'Herbomez M, Monpeyssen H, Tramalloni J, Leteurtre E, et al. . Guidelines of the French society of endocrinology for the management of thyroid nodules. Ann Endocrinol. (2011) 72:251–81. 10.1016/j.ando.2011.05.003
    1. Frates MC, Benson CB, Charboneau JW, Cibas ES, Clark OH, Coleman BG, et al. . Management of thyroid nodules detected at US: Society of Radiologists in Ultrasound consensus conference statement. Radiology. (2005) 237:794–800. 10.1148/radiol.2373050220
    1. Tuttle RM, Haddad RI, Ball DW, Byrd D, Dickson P, Duh QY, et al. Thyroid carcinoma, version 2.2014. J Natl Comp Cancer Netw. (2014) 12:1671–80; quiz 80. 10.6004/jnccn.2014.0169
    1. Yoon JH, Lee HS, Kim EK, Moon HJ, Kwak JY. Malignancy risk stratification of thyroid nodules: comparison between the thyroid imaging reporting and data system and the 2014 American Thyroid Association Management Guidelines. Radiology. (2016) 278:917–24. 10.1148/radiol.2015150056
    1. Gharib H, Papini E, Garber JR, Duick DS, Harrell RM, Hegedus L, et al. American association of clinical endocrinologists, American college of endocrinology, and associazione medici endocrinologi medical guidelines for clinical practice for the diagnosis and management of thyroid nodules−2016 update. Endocr Pract. (2016) 22:622–39. 10.4158/
    1. 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. 10.1089/thy.2015.0020
    1. Perros P, Boelaert K, Colley S, Evans C, Evans RM, Gerrard Ba G, et al. . Guidelines for the management of thyroid cancer. Clin Endocrinol. (2014) 81(Suppl 1):1–122. 10.1111/cen.12515
    1. Persichetti A, Di Stasio E, Guglielmi R, Bizzarri G, Taccogna S, Misischi I, et al. . Predictive value of malignancy of thyroid nodule ultrasound classification systems: a prospective study. J Clin Endocrinol Metab. (2018) 103:1359–68. 10.1210/jc.2017-01708
    1. Lauria Pantano A, Maddaloni E, Briganti SI, Beretta Anguissola G, Perrella E, Taffon C, 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. 10.1530/EJE-18-0083
    1. Ha EJ, Na DG, Baek JH, Sung JY, Kim JH, Kang SY. US fine-needle aspiration biopsy for thyroid malignancy: diagnostic performance of seven society guidelines applied to 2000 thyroid nodules. Radiology. (2018) 287:893–900. 10.1148/radiol.2018171074
    1. Ha EJ, Na DG, Moon WJ, Lee YH, Choi N. Diagnostic performance of ultrasound-based risk-stratification systems for thyroid nodules: comparison of the 2015 American Thyroid Association Guidelines with the. 2016 Korean Thyroid Association/Korean Society of Thyroid Radiology and 2017 American Congress of Radiology Guidelines. Thyroid. (2018). 28:1532–7. 10.1089/thy.2018.0094
    1. Trimboli P, Durante C. Ultrasound risk stratification systems for thyroid nodule: between lights and shadows, we are moving towards a new era. Endocrine. (2020). 10.1007/s12020-020-02196-6. [Epub ahead of print].
    1. Fadda G, Basolo F, Bondi A, Bussolati G, Crescenzi A, Nappi O, et al. . Cytological classification of thyroid nodules. Proposal of the SIAPEC-IAP Italian Consensus Working Group. Pathologica. (2010) 102:405–8.
    1. Persichetti A, Di Stasio E, Coccaro C, Graziano F, Bianchini A, Di Donna V, et al. . Inter- and intraobserver agreement in the assessment of thyroid nodule ultrasound features and classification systems: a blinded multicenter study. Thyroid. (2020) 30:237–42. 10.1089/thy.2019.0360
    1. Lam CA, McGettigan MJ, Thompson ZJ, Khazai L, Chung CH, Centeno BA, et al. . Ultrasound characterization for thyroid nodules with indeterminate cytology: inter-observer agreement and impact of combining pattern-based and scoring-based classifications in risk stratification. Endocrine. (2019) 66:278–87. 10.1007/s12020-019-02000-0
    1. Cohen J. A coefficient of agreement for nominal scales. Educ Psychol Meas. (1960) 20:37–46. 10.1177/001316446002000104
    1. Sprent P, Smeeton NC. (eds.). Applied Nonparametric Statistical Methods. London: Chapman & Hall; CRC; (2001).
    1. Macedo BM, Izquierdo RF, Golbert L, Meyer ELS. Reliability of thyroid imaging reporting and data system (TI-RADS), and ultrasonographic classification of the American Thyroid Association (ATA) in differentiating benign from malignant thyroid nodules. Arch Endocrinol Metab. (2018) 62:131–8. 10.20945/2359-3997000000018
    1. Pandya A, Caoili EM, Jawad-Makki F, Wasnik AP, Shankar PR, Bude R, et al. . Limitations of the 2015 ATA guidelines for prediction of thyroid cancer: a review of 1947 consecutive aspirations. J Clin Endocrinol Metab. (2018). 103:3496–502. 10.1210/jc.2018-00792
    1. Choi SH, Kim EK, Kwak JY, Kim MJ, Son EJ. Interobserver and intraobserver variations in ultrasound assessment of thyroid nodules. Thyroid. (2010) 20:167–72. 10.1089/thy.2008.0354
    1. Scappaticcio L, Virili C, Castellana M, Paone G, Centanni M, Trimboli P, et al. . An unsuspicious thyroid nodule with fatal outcome. Hormones (Athens). (2019) 18:321–4. 10.1007/s42000-019-00110-y

Source: PubMed

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