{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,3]],"date-time":"2026-10-03T04:20:57Z","timestamp":1791001257809,"version":"4.1.0"},"reference-count":22,"publisher":"Springer Science and Business Media LLC","issue":"2","license":[{"start":{"date-parts":[[2021,6,12]],"date-time":"2021-06-12T00:00:00Z","timestamp":1623456000000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2021,6,12]],"date-time":"2021-06-12T00:00:00Z","timestamp":1623456000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"funder":[{"name":"National Center for Research and Development","award":["STRATEGMED2\/267398\/4\/NCBR\/2015"],"award-info":[{"award-number":["STRATEGMED2\/267398\/4\/NCBR\/2015"]}]}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Endocrine"],"published-print":{"date-parts":[[2021,11]]},"abstract":"<jats:title>Abstract<\/jats:title><jats:sec>\n                <jats:title>Purpose<\/jats:title>\n                <jats:p>Equivocal categories (III, IV, V) of the Bethesda System for Reporting Thyroid Cytology (BSRTC) are characterized by high variability of the estimated risk of malignancy. The aim of the study was to analyze the reproducibility of classification of nodules into an equivocal category and the frequency of malignancy (FoM) observed in such categories.<\/jats:p>\n              <\/jats:sec><jats:sec>\n                <jats:title>Methods<\/jats:title>\n                <jats:p>Five experienced cytopathologists from three centers (A, B, C) independently performed reclassification of smears obtained from 213 thyroid nodules with equivocal routine cytology and known results of the postoperative histopathological examination.<\/jats:p>\n              <\/jats:sec><jats:sec>\n                <jats:title>Results<\/jats:title>\n                <jats:p>The interobserver agreement among all cytopathologists was poor, with a Krippendorff\u2019s alpha coefficient equaling 0.34. The intra-center agreement was higher than the inter-center (fair vs poor). Pathologists of the center A classified smears into categories II and III significantly less often and categories IV and V more often than pathologists of centers B and C. The joint FoM of nodules classified into any of categories IV\u2013VI (regarded as an indication for surgery) was different among centers (A: 40.0%, B: 66.7%, C: 80.6%). The FoM of category III nodules with features of nuclear atypia (AUS) in center B and C was two times higher than that of other nodules of category III (FLUS), while in center A the FoM was similar.<\/jats:p>\n              <\/jats:sec><jats:sec>\n                <jats:title>Conclusions<\/jats:title>\n                <jats:p>The use of published data on the risk of malignancy in nodules of particular BSRTC categories without concern for the uniqueness of the diagnostic center may lead to erroneous conclusions.<\/jats:p>\n              <\/jats:sec>","DOI":"10.1007\/s12020-021-02781-3","type":"journal-article","created":{"date-parts":[[2021,6,12]],"date-time":"2021-06-12T07:02:30Z","timestamp":1623481350000},"page":"355-364","update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":21,"title":["Low reproducibility of equivocal categories of the Bethesda System for Reporting Thyroid Cytology makes the associated risk of malignancy specific to the diagnostic center"],"prefix":"10.1007","volume":"74","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-5617-0418","authenticated-orcid":false,"given":"Dorota","family":"S\u0142owi\u0144ska-Klencka","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mariusz","family":"Klencki","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Joanna","family":"Duda-Szyma\u0144ska","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jaros\u0142aw","family":"Szwalski","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Bo\u017cena","family":"Popowicz","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2021,6,12]]},"reference":[{"key":"2781_CR1","doi-asserted-by":"publisher","first-page":"658","DOI":"10.1309\/AJCPPHLWMI3JV4LA","volume":"132","author":"ES Cibas","year":"2009","unstructured":"E.S. Cibas, S.Z. Ali, NCI Thyroid FNA State of the Science Conference. The Bethesda system for reporting thyroid cytopathology. Am. J. Clin. Pathol. 132, 658\u2013665 (2009). https:\/\/doi.org\/10.1309\/AJCPPHLWMI3JV4LA","journal-title":"Am. J. Clin. Pathol."},{"key":"2781_CR2","doi-asserted-by":"publisher","first-page":"1341","DOI":"10.1089\/thy.2017.0500","volume":"27","author":"ES Cibas","year":"2017","unstructured":"E.S. Cibas, S.Z. Ali, The 2017 Bethesda system for reporting thyroid cytopathology. Thyroid 27, 1341\u20131346 (2017). https:\/\/doi.org\/10.1089\/thy.2017.0500","journal-title":"Thyroid"},{"key":"2781_CR3","doi-asserted-by":"publisher","first-page":"238","DOI":"10.1002\/cncy.22228","volume":"128","author":"HG Vuong","year":"2020","unstructured":"H.G. Vuong, H.T.T. Ngo, A. Bychkov, C.K. Jung, T.H. Vu, K.B. Lu, K. Kakudo, T. Kondo, Differences in surgical resection rate and risk of malignancy in thyroid cytopathology practice between Western and Asian countries: a systematic review and meta-analysis. Cancer Cytopathol. 128, 238\u2013249 (2020). https:\/\/doi.org\/10.1002\/cncy.22228","journal-title":"Cancer Cytopathol."},{"key":"2781_CR4","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1089\/thy.2015.0020","volume":"26","author":"BR Haugen","year":"2016","unstructured":"B.R. Haugen, E.K. Alexander, K.C. Bible, G.M. Doherty, S.J. Mandel, Y.E. Nikiforov, F. Pacini, G.W. Randolph, A.M. Sawka, M. Schlumberger, K.G. Schuff, S.I. Sherman, J.A. Sosa, D.L. Steward, R.M. Tuttle, L. Wartofsky, 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 26, 1\u2013133 (2016). https:\/\/doi.org\/10.1089\/thy.2015.0020","journal-title":"Thyroid"},{"key":"2781_CR5","doi-asserted-by":"publisher","first-page":"115","DOI":"10.1159\/000468519","volume":"6","author":"R Paschke","year":"2017","unstructured":"R. Paschke, S. Cantara, A. Crescenzi, B. Jarzab, T.J. Musholt, M. Sobrinho Simoes, European thyroid association guidelines regarding thyroid nodule molecular fine-needle aspiration cytology diagnostics. Eur. Thyroid J. 6, 115\u2013129 (2017). https:\/\/doi.org\/10.1159\/000468519","journal-title":"Eur. Thyroid J."},{"key":"2781_CR6","doi-asserted-by":"publisher","first-page":"481","DOI":"10.1002\/cncy.21412","volume":"122","author":"M Nishino","year":"2014","unstructured":"M. Nishino, H.H. Wang, Should the thyroid AUS\/FLUS category be further stratified by malignancy risk? Cancer Cytopathol. 122, 481\u2013483 (2014). https:\/\/doi.org\/10.1002\/cncy.21412","journal-title":"Cancer Cytopathol."},{"key":"2781_CR7","doi-asserted-by":"publisher","first-page":"3913","DOI":"10.1245\/s10434-018-6826-6","volume":"25","author":"N Eisa","year":"2018","unstructured":"N. Eisa, A. Khan, M. Akhter, M. Fensterwald, S. Saleem, G. Fananapazir, M.J. Campbell, Both ultrasound features and nuclear atypia are associated with malignancy in thyroid nodules with atypia of undetermined significance. Ann. Surg. Oncol. 25, 3913\u20133918 (2018). https:\/\/doi.org\/10.1245\/s10434-018-6826-6","journal-title":"Ann. Surg. Oncol."},{"key":"2781_CR8","doi-asserted-by":"publisher","first-page":"368","DOI":"10.1002\/cncy.21396","volume":"122","author":"J Hyeon","year":"2014","unstructured":"J. Hyeon, S. Ahn, J.H. Shin, Y.L. Oh, The prediction of malignant risk in the category \u201catypia of undetermined significance\/follicular lesion of undetermined significance\u201d of the Bethesda system for reporting thyroid cytopathology using subcategorization and BRAF mutation results. Cancer Cytopathol. 122, 368\u2013376 (2014). https:\/\/doi.org\/10.1002\/cncy.21396","journal-title":"Cancer Cytopathol."},{"key":"2781_CR9","doi-asserted-by":"publisher","first-page":"1471","DOI":"10.1016\/j.surg.2014.08.026","volume":"156","author":"A Mathur","year":"2014","unstructured":"A. Mathur, A. Najafian, E.B. Schneider, M.A. Zeiger, M.T. Olson, Malignancy risk and reproducibility associated with atypia of undetermined significance on thyroid cytology. Surgery 156, 1471\u20131476 (2014). https:\/\/doi.org\/10.1016\/j.surg.2014.08.026","journal-title":"Surgery"},{"key":"2781_CR10","doi-asserted-by":"publisher","first-page":"65","DOI":"10.1111\/cyt.12352","volume":"28","author":"SJ Kim","year":"2017","unstructured":"S.J. Kim, J. Roh, J.H. Baek, S.J. Hong, Y.K. Shong, W.B. Kim, D.E. Song, Risk of malignancy according to sub-classification of the atypia of undetermined significance or follicular lesion of undetermined significance (AUS\/FLUS) category in the Bethesda system for reporting thyroid cytopathology. Cytopathology 28, 65\u201373 (2017). https:\/\/doi.org\/10.1111\/cyt.12352","journal-title":"Cytopathology"},{"key":"2781_CR11","doi-asserted-by":"publisher","first-page":"1764","DOI":"10.21037\/gs-20-555","volume":"9","author":"LY Ooi","year":"2020","unstructured":"L.Y. Ooi, M.E. Nga, Atypia of undetermined significance\/follicular lesion of undetermined significance: Asian vs. non-Asian practice, and the Singapore experience. Gland Surg. 9, 1764\u20131787 (2020). https:\/\/doi.org\/10.21037\/gs-20-555","journal-title":"Gland Surg."},{"key":"2781_CR12","doi-asserted-by":"publisher","first-page":"621","DOI":"10.1530\/EJE-12-0993","volume":"168","author":"D S\u0142owi\u0144ska-Klencka","year":"2013","unstructured":"D. S\u0142owi\u0144ska-Klencka, E. Wo\u017aniak, M. Wojtaszek, B. Popowicz, S. Sporny, M. Klencki, Low malignancy risk of thyroid follicular lesion of undetermined significance in patients from post-endemic areas. Eur. J. Endocrinol. 168, 621\u2013630 (2013). https:\/\/doi.org\/10.1530\/EJE-12-0993","journal-title":"Eur. J. Endocrinol."},{"key":"2781_CR13","doi-asserted-by":"publisher","first-page":"77","DOI":"10.1080\/19312450709336664","volume":"1","author":"AF Hayes","year":"2007","unstructured":"A.F. Hayes, K. Krippendorff, Answering the call for a standard reliability measure for coding data. Commun. Methods Measures 1, 77\u201389 (2007)","journal-title":"Commun. Methods Measures"},{"key":"2781_CR14","doi-asserted-by":"publisher","first-page":"767","DOI":"10.7863\/ultra.34.5.767","volume":"34","author":"A Kamaya","year":"2015","unstructured":"A. Kamaya, G.H. Lewis, Y. Liu, H. Akatsu, C. Kong, T.S. Desser, Atypia of undetermined significance and follicular lesions of undetermined significance: sonographic assessment for prediction of the final diagnosis. J. Ultrasound Med. 34, 767\u2013774 (2015). https:\/\/doi.org\/10.7863\/ultra.34.5.767","journal-title":"J. Ultrasound Med."},{"key":"2781_CR15","doi-asserted-by":"publisher","first-page":"1115","DOI":"10.1089\/thy.2013.0650","volume":"24","author":"PW Rosario","year":"2014","unstructured":"P.W. Rosario, Thyroid nodules with atypia or follicular lesions of undetermined significance (Bethesda Category III): importance of ultrasonography and cytological subcategory. Thyroid 24, 1115\u20131120 (2014). https:\/\/doi.org\/10.1089\/thy.2013.0650","journal-title":"Thyroid"},{"key":"2781_CR16","doi-asserted-by":"publisher","first-page":"1037","DOI":"10.1002\/dc.21702","volume":"40","author":"X Jing","year":"2012","unstructured":"X. Jing, S.M. Knoepp, M.H. Roh, K. Hookim, J. Placido, R. Davenport, R. Rasche, C.W. Michael, Group consensus review minimizes the diagnosis of \u201cfollicular lesion of undetermined significance\u201d and improves cytohistologic concordance. Diagn. Cytopathol. 40, 1037\u20131042 (2012). https:\/\/doi.org\/10.1002\/dc.21702","journal-title":"Diagn. Cytopathol."},{"key":"2781_CR17","doi-asserted-by":"publisher","first-page":"507","DOI":"10.1159\/000334687","volume":"55","author":"B Cochand-Priollet","year":"2011","unstructured":"B. Cochand-Priollet, F.C. Schmitt, M. T\u00f6tsch, P. Vielh, European Federation of Cytology Societies\u2019 Scientific Committee. The Bethesda terminology for reporting thyroid cytopathology: from theory to practice in Europe. Acta Cytol. 55, 507\u2013511 (2011). https:\/\/doi.org\/10.1159\/000334687","journal-title":"Acta Cytol."},{"key":"2781_CR18","unstructured":"S. Ahmed, M. Ahmad, M.A. Khan, F. Kazi, F. Noreen, S. Nawaz, I. Sohail. The interobserver reproducibility of thyroid cytopathology using Bethesda Reporting System: analysis of 200 cases. J. Pak. Med. Assoc. 63, 1252\u20131255 (2013)"},{"key":"2781_CR19","doi-asserted-by":"publisher","first-page":"33","DOI":"10.4103\/JOC.JOC_215_16","volume":"35","author":"P Awasthi","year":"2018","unstructured":"P. Awasthi, G. Goel, U. Khurana, D. Joshi, K. Majumdar, N. Kapoor, Reproducibility of \u201cThe Bethesda System for Reporting Thyroid Cytopathology:\u201d a retrospective analysis of 107 patients. J. Cytol. 35, 33\u201336 (2018). https:\/\/doi.org\/10.4103\/JOC.JOC_215_16","journal-title":"J. Cytol."},{"key":"2781_CR20","doi-asserted-by":"publisher","first-page":"852","DOI":"10.1309\/AJCPZ33MVMGZKEWU","volume":"135","author":"G Kocjan","year":"2011","unstructured":"G. Kocjan, A. Chandra, P.A. Cross, T. Giles, S.J. Johnson, T.J. Stephenson, M. Roughton, D.N. Poller, The interobserver reproducibility of thyroid fine-needle aspiration using the UK Royal College of Pathologists\u2019 classification system. Am. J. Clin. Pathol. 135, 852\u2013859 (2011). https:\/\/doi.org\/10.1309\/AJCPZ33MVMGZKEWU","journal-title":"Am. J. Clin. Pathol."},{"key":"2781_CR21","doi-asserted-by":"publisher","first-page":"399","DOI":"10.1002\/dc.23681","volume":"45","author":"V Padmanabhan","year":"2017","unstructured":"V. Padmanabhan, C.B. Marshall, G. Akdas Barkan, M. Ghofrani, A. Laser, I. Tolgay Oca, C. David Sturgis, R. Souers, D.F. Kurtycz, 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\u2013405 (2017). https:\/\/doi.org\/10.1002\/dc.23681","journal-title":"Diagn. Cytopathol."},{"key":"2781_CR22","doi-asserted-by":"publisher","first-page":"1051","DOI":"10.7860\/JCDR\/2013\/5754.3087","volume":"7","author":"TM Bhasin","year":"2013","unstructured":"T.M. Bhasin, R. Mannan, M. Manjari, M. Mehra, A.K. Gill Sekhon, M. Chandey, S. Sharma, P. Kaur, Reproducibility of \u2018The Bethesda System for reporting Thyroid Cytopathology\u2019: a multicenter study with review of the literature. J. Clin. Diagn. Res. 7, 1051\u20131054 (2013). https:\/\/doi.org\/10.7860\/JCDR\/2013\/5754.3087","journal-title":"J. Clin. Diagn. Res."}],"container-title":["Endocrine"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1007\/s12020-021-02781-3.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/article\/10.1007\/s12020-021-02781-3\/fulltext.html","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1007\/s12020-021-02781-3.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2021,10,8]],"date-time":"2021-10-08T06:54:36Z","timestamp":1633676076000},"score":1,"resource":{"primary":{"URL":"https:\/\/link.springer.com\/10.1007\/s12020-021-02781-3"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,6,12]]},"references-count":22,"journal-issue":{"issue":"2","published-print":{"date-parts":[[2021,11]]}},"alternative-id":["2781"],"URL":"https:\/\/doi.org\/10.1007\/s12020-021-02781-3","relation":{},"ISSN":["1355-008X","1559-0100"],"issn-type":[{"value":"1355-008X","type":"print"},{"value":"1559-0100","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,6,12]]},"assertion":[{"value":"18 April 2021","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"25 May 2021","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"12 June 2021","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Compliance with ethical standards"}},{"value":"The authors declare no competing interests.","order":2,"name":"Ethics","group":{"name":"EthicsHeading","label":"Conflict of interest"}},{"value":"The study design was approved by the Local Bioethics Committee at the National Research Institute of Oncology - as a part of the studies carried out for the realization of the grant MILESTONE. The approval code is \u201c13\/2015\/1\/2016\u201d.","order":3,"name":"Ethics","group":{"name":"EthicsHeading","label":"Ethical approval"}},{"value":"All patients subjected to FNA of the thyroid gland gave their informed consent.","order":4,"name":"Ethics","group":{"name":"EthicsHeading","label":"Consent to participate"}}]}}