Validating the 'CUT score' risk stratification tool for indeterminate thyroid nodules using the Bethesda system for reporting thyroid cytopathology.
BSRTC
Indeterminate
Risk of malignancy
Scoring system
Thyroid nodule
Ultrasonography
Journal
European archives of oto-rhino-laryngology : official journal of the European Federation of Oto-Rhino-Laryngological Societies (EUFOS) : affiliated with the German Society for Oto-Rhino-Laryngology - Head and Neck Surgery
ISSN: 1434-4726
Titre abrégé: Eur Arch Otorhinolaryngol
Pays: Germany
ID NLM: 9002937
Informations de publication
Date de publication:
Jan 2022
Jan 2022
Historique:
received:
09
01
2021
accepted:
23
03
2021
pubmed:
13
4
2021
medline:
11
1
2022
entrez:
12
4
2021
Statut:
ppublish
Résumé
Managing intermediate thyroid nodules remains challenging. The CUT score is an Italian metanalysis-based cytologic (SIAPEC-IAP) scoring system, designed to assist clinicians. However, it was never evaluated against the Bethesda system for reporting thyroid cytopathology (BSRTC). This study aims to validate its utility for BSRTC III and IV nodules in a non-Italian population. We collected all BSRTC III and IV thyroid nodules with a documented final pathology between 2010 and 2020. We calculated the C + U components of the CUT score using retrospective clinical (C) data collection and reevaluation of preoperative sonography (U) examination. The cytology (T) component which originally referred to the five-tiered SIAPEC-IAP cytologic classification was replaced by the corresponding BSRTC categories. Optimal test performances were calculated using receiver operating characteristic (ROC) curve analysis. Data were analyzed twice with considering of NIFTP as benign and as malignant. After exclusions, 62 nodules from 61 patients were included (50% BSRTC III, 50% BSRTC IV). Malignant nodules demonstrated a significantly higher C + U score compared with benign in both categories. The C + U cutoff value for BSRTC III was 5.25 (sensitivity and specificity of 69.23% and 66.67%, respectively, AUC = 0.72, p-value = 0.016), and 5.75 for BSRTC IV (sensitivity and specificity of 85.7% and 76.5%, respectively, AUC = 0.84, p-value < 0.001). Our study suggests that the CUT score is applicable for both BSRTC III and IV nodules, and highlights the need for internal validations, since the cutoffs found were higher than previously reported.
Identifiants
pubmed: 33844064
doi: 10.1007/s00405-021-06783-9
pii: 10.1007/s00405-021-06783-9
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
383-390Informations de copyright
© 2021. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.
Références
Gharib H, Papini E, Garber JR, Duick DS, Harrell RM, Hegedüs L et al (2016) 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 22:1–60
Gharib H, Papini E (2007) Thyroid nodules: clinical importance, assessment, and treatment. Endocrinol Metab Clin North Am 36(707–35):vi
Rosato L, Avenia N, Bernante P, De Palma M, Gulino G, Nasi PG et al (2004) Complications of thyroid surgery: analysis of a multicentric study on 14,934 patients operated on in Italy over 5 years. World J Surg 28:271–276
pubmed: 14961204
pmcid: 14961204
Jeannon J-P, Orabi AA, Bruch GA, Abdalsalam HA, Simo R (2009) Diagnosis of recurrent laryngeal nerve palsy after thyroidectomy: a systematic review. Int J Clin Pract 63:624–629
pubmed: 19335706
pmcid: 19335706
Cibas ES, Ali SZ (2009) The Bethesda system for reporting thyroid cytopathology. Thyroid Off J Am Thyroid Assoc 19:1159–1165
Cibas ES, Ali SZ (2017) The 2017 Bethesda system for reporting thyroid cytopathology. Thyroid 27:1341–1346
pubmed: 29091573
pmcid: 29091573
Cooper DS, Doherty GM, Haugen BR, Kloos RT, Lee SL, Mandel SJ et al (2006) Management guidelines for patients with thyroid nodules and differentiated thyroid cancer. Thyroid Off J Am Thyroid Assoc 16:109–142
Greaves TS, Olvera M, Florentine BD, Raza AS, Cobb CJ, Tsao-Wei DD et al (2000) Follicular lesions of thyroid: a 5-year fine-needle aspiration experience. Cancer 90:335–341
pubmed: 11156516
pmcid: 11156516
Sclabas GM, Staerkel GA, Shapiro SE, Fornage BD, Sherman SI, Vassillopoulou-Sellin R et al (2003) Fine-needle aspiration of the thyroid and correlation with histopathology in a contemporary series of 240 patients. Am J Surg 186:702–709 ((Discussion 709-710))
pubmed: 14672783
pmcid: 14672783
Nikiforov YE, Steward DL, Robinson-Smith TM, Haugen BR, Klopper JP, Zhu Z et al (2009) Molecular testing for mutations in improving the fine-needle aspiration diagnosis of thyroid nodules. J Clin Endocrinol Metab 94:2092–2098
pubmed: 19318445
pmcid: 19318445
Chudova D, Wilde JI, Wang ET, Wang H, Rabbee N, Egidio CM et al (2010) Molecular classification of thyroid nodules using high-dimensionality genomic data. J Clin Endocrinol Metab 95:5296–5304
pubmed: 20826580
pmcid: 20826580
Kloos RT, Reynolds JD, Walsh PS, Wilde JI, Tom EY, Pagan M et al (2013) Does addition of BRAF V600E mutation testing modify sensitivity or specificity of the Afirma gene expression classifier in cytologically indeterminate thyroid nodules? J Clin Endocrinol Metab 98:E761-768
pubmed: 23476074
pmcid: 23476074
Tonacchera M, Agretti P, Rago T, De Marco G, Niccolai F, Molinaro A et al (2012) Genetic markers to discriminate benign and malignant thyroid nodules with undetermined cytology in an area of borderline iodine deficiency. J Endocrinol Invest 35:754–759
pubmed: 21979329
pmcid: 21979329
Alexander EK, Kennedy GC, Baloch ZW, Cibas ES, Chudova D, Diggans J et al (2012) Preoperative diagnosis of benign thyroid nodules with indeterminate cytology. N Engl J Med 367:705–715
pubmed: 22731672
pmcid: 22731672
Brauner E, Holmes BJ, Krane JF, Nishino M, Zurakowski D, Hennessey JV et al (2015) Performance of the Afirma gene expression classifier in Hurthle cell thyroid nodules differs from other indeterminate thyroid nodules. Thyroid Off J Am Thyroid Assoc 25:789–796
Marti JL, Avadhani V, Donatelli LA, Niyogi S, Wang B, Wong RJ et al (2015) Wide inter-institutional variation in performance of a molecular classifier for indeterminate thyroid nodules. Ann Surg Oncol 22:3996–4001
pubmed: 25862581
pmcid: 25862581
Alexander EK, Schorr M, Klopper J, Kim C, Sipos J, Nabhan F et al (2014) Multicenter clinical experience with the Afirma gene expression classifier. J Clin Endocrinol Metab 99:119–125
pubmed: 24152684
pmcid: 24152684
McIver B, Castro MR, Morris JC, Bernet V, Smallridge R, Henry M et al (2014) An independent study of a gene expression classifier (Afirma) in the evaluation of cytologically indeterminate thyroid nodules. J Clin Endocrinol Metab 99:4069–4077
pubmed: 24780044
pmcid: 24780044
Wu JX, Lam R, Levin M, Rao J, Sullivan PS, Yeh MW (2016) Effect of malignancy rates on cost-effectiveness of routine gene expression classifier testing for indeterminate thyroid nodules. Surgery 159:118–126
pubmed: 26435428
pmcid: 26435428
Tumino D, Grani G, Di Stefano M, Di Mauro M, Scutari M, Rago T et al (2020) Nodular thyroid disease in the era of precision medicine. Front Endocrinol 10:907
Liu YI, Kamaya A, Desser TS, Rubin DL (2011) A bayesian network for differentiating benign from malignant thyroid nodules using sonographic and demographic features. AJR Am J Roentgenol 196:W598-605
pubmed: 21512051
pmcid: 21512051
Kwak JY, Han KH, Yoon JH, Moon HJ, Son EJ, Park SH et al (2011) Thyroid imaging reporting and data system for US features of nodules: a step in establishing better stratification of cancer risk. Radiology 260:892–899
pubmed: 21771959
pmcid: 21771959
Cantisani V, D’Andrea V, Mancuso E, Maggini E, Di Segni M, Olive M et al (2013) Prospective evaluation in 123 patients of strain ratio as provided by quantitative elastosonography and multiparametric ultrasound evaluation (ultrasound score) for the characterisation of thyroid nodules. Radiol Med (Torino) 118:1011–1021
Sands NB, Karls S, Amir A, Tamilia M, Gologan O, Rochon L et al (2011) McGill Thyroid Nodule Score (MTNS): “rating the risk”, a novel predictive scheme for cancer risk determination. J Otolaryngol Head Neck Surg J Oto-Rhino-Laryngol Chir Cervico-Faciale 40(Suppl 1):S1-13
Camargo RY, Tomimori EK, Knobel M, Medeiros-Neto G (2007) Preoperative assessment of thyroid nodules: role of ultrasonography and fine needle aspiration biopsy followed by cytology. Clinics 62:411–418
pubmed: 17823703
pmcid: 17823703
Russ G, Royer B, Bigorgne C, Rouxel A, Bienvenu-Perrard M, Leenhardt L (2013) Prospective evaluation of thyroid imaging reporting and data system on 4550 nodules with and without elastography. Eur J Endocrinol 168:649–655
pubmed: 23416955
pmcid: 23416955
Ianni F, Campanella P, Rota CA, Prete A, Castellino L, Pontecorvi A et al (2016) A meta-analysis-derived proposal for a clinical, ultrasonographic, and cytological scoring system to evaluate thyroid nodules: the “CUT” score. Endocrine 52:313–321
pubmed: 26518189
pmcid: 26518189
Fadda G, Basolo F, Bondi A, Bussolati G, Crescenzi A, Nappi O et al (2010) Cytological classification of thyroid nodules. Proposal of the SIAPEC-IAP Italian Consensus Working Group. Pathologica 102:405–408
pubmed: 21361121
pmcid: 21361121
Ianni F, Pascucci D, Paragliola RM, Rota CA, Perotti G, Fadda G et al (2020) Follow-Up or surgery for indeterminate thyroid nodules: could the CUT score application be a support for decision-making in the preoperative assessment? Thyroid 30:65–71
pubmed: 31552809
pmcid: 31552809
Nardi F, Basolo F, Crescenzi A, Fadda G, Frasoldati A, Orlandi F et al (2014) Italian consensus for the classification and reporting of thyroid cytology. J Endocrinol Invest 37:593–599
pubmed: 24789536
pmcid: 24789536
Campanella P, Ianni F, Rota CA, Corsello SM, Pontecorvi A (2014) Quantification of cancer risk of each clinical and ultrasonographic suspicious feature of thyroid nodules: a systematic review and meta-analysis. Eur J Endocrinol 170:R203-211
pubmed: 24536085
pmcid: 24536085
Hirsch D, Robenshtok E, Bachar G, Braslavsky D, Benbassat C (2015) The implementation of the bethesda system for reporting thyroid cytopathology improves malignancy detection despite lower rate of thyroidectomy in indeterminate nodules. World J Surg 39:1959–1965
pubmed: 25809059
pmcid: 25809059
Ke J, Jianyong L, Ying L, Genpeng L, Linlin S, Zhihui L et al (2019) The use of The Bethesda system for reporting thyroid cytopathology in a chinese population: an analysis of 13 351 specimens. Diagn Cytopathol 47:876–880
pubmed: 31074206
pmcid: 31074206
Ronen O, Cohen H, Abu M (2019) Review of a single institution’s fine needle aspiration results for thyroid nodules: initial observations and lessons for the future. Cytopathology 30:468–474
pubmed: 31206845
pmcid: 31206845
Park JH, Yoon SO, Son EJ, Kim HM, Nahm JH, Hong S (2014) Incidence and malignancy rates of diagnoses in the bethesda system for reporting thyroid aspiration cytology: an institutional experience. Korean J Pathol 48:133
pubmed: 24868226
pmcid: 24868226
Abu-Ghanem S, Cohen O, Raz Yarkoni T, Fliss DM, Yehuda M (2016) intraoperative frozen section in “suspicious for papillary thyroid carcinoma” after adoption of the Bethesda system. Otolaryngol Neck Surg 155:779–786
Haugen BR, Alexander EK, Bible KC, Doherty GM, Mandel SJ, Nikiforov YE et al (2016) 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 Off J Am Thyroid Assoc 26:1–133
Cooper DS, Doherty GM, Haugen BR, Kloos RT, Lee SL, Mandel SJ et al (2009) Revised American thyroid association management guidelines for patients with thyroid nodules and differentiated thyroid cancer. Thyroid Off J Am Thyroid Assoc 19:1167–1214
Baloch ZW, LiVolsi VA, Asa SL, Rosai J, Merino MJ, Randolph G et al (2008) Diagnostic terminology and morphologic criteria for cytologic diagnosis of thyroid lesions: a synopsis of the National Cancer Institute Thyroid Fine-Needle Aspiration State of the Science Conference. Diagn Cytopathol 36:425–437
pubmed: 18478609
pmcid: 18478609
Choi SH, Kim E-K, Kwak JY, Kim MJ, Son EJ (2010) Interobserver and intraobserver variations in ultrasound assessment of thyroid nodules. Thyroid Off J Am Thyroid Assoc 20:167–172
Straccia P, Rossi ED, Bizzarro T, Brunelli C, Cianfrini F, Damiani D et al (2015) A meta-analytic review of the Bethesda system for reporting thyroid cytopathology: has the rate of malignancy in indeterminate lesions been underestimated?: TBSRTC for Indeterminate Lesions. Cancer Cytopathol 123:713–722
pubmed: 26355876
pmcid: 26355876
Padmanabhan V, Marshall CB, Akdas Barkan G, Ghofrani M, Laser A, Tolgay Ocal I et al (2017) Reproducibility of atypia of undetermined significance/follicular lesion of undetermined significance category using the bethesda system for reporting thyroid cytology when reviewing slides from different institutions: a study of interobserver variability among cytopathologists. Diagn Cytopathol 45:399–405
pubmed: 28217980
pmcid: 28217980
Olson MT, Boonyaarunnate T, Aragon Han P, Umbricht CB, Ali SZ, Zeiger MA (2013) A tertiary center’s experience with second review of 3885 thyroid cytopathology specimens. J Clin Endocrinol Metab 98:1450–1457
pubmed: 23436916
pmcid: 23436916
Cohen O, Tzelnick S, Lahav Y, Schindel D, Halperin D, Yehuda M (2017) Selection of atypia/follicular lesion of unknown significance patients for surgery versus active surveillance, without using genetic testing: a single institute experience, prospective analysis, and recommendations. Thyroid 27:928–935
pubmed: 28463595
pmcid: 28463595
Ho AS, Sarti EE, Jain KS, Wang H, Nixon IJ, Shaha AR et al (2014) Malignancy rate in thyroid nodules classified as Bethesda category III (AUS/FLUS). Thyroid Off J Am Thyroid Assoc 24:832–839