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Review Article| Volume 16, ISSUE 1, P1-14, March 2023

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A Triumvirate:

Correlating Thyroid Cytopathology, Molecular Testing, and Histopathology
Published:December 08, 2022DOI:https://doi.org/10.1016/j.path.2022.09.003

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      References

        • Cibas E.S.
        • Ali S.Z.
        The 2017 bethesda system for reporting thyroid cytopathology.
        J Am Soc Cytopathol. 2017; 6: 217-222
        • Rossi E.D.
        • Adeniran A.J.
        • Faquin W.C.
        Pitfalls in thyroid cytopathology.
        Surg Pathol Clin. 2019; 12: 865-881
        • Juhlin C.C.
        • Stenman A.
        • Zedenius J.
        Macrofollicular variant follicular thyroid tumors are DICER1 mutated and exhibit distinct histological features.
        Histopathology. 2021; 79: 661-666
        • Policarpio-Nicolas M.L.
        • Sirohi D.
        Macrofollicular variant of papillary carcinoma, a potential diagnostic pitfall: a report of two cases including a review of literature.
        Cytojournal. 2013; 10: 16
        • Nikiforova M.N.
        • Mercurio S.
        • Wald A.I.
        • et al.
        Analytical performance of the ThyroSeq v3 genomic classifier for cancer diagnosis in thyroid nodules.
        Cancer. 2018; 124: 1682-1690
        • Ohori N.P.
        • Landau M.S.
        • Carty S.E.
        • et al.
        Benign call rate and molecular test result distribution of ThyroSeq v3.
        Cancer Cytopathol. 2019; 127: 161-168
        • Bose S.
        • Sacks W.
        • Walts A.E.
        Update on molecular testing for cytologically indeterminate thyroid nodules.
        Adv Anat Pathol. 2019; 26: 114-123
        • Bongiovanni M.
        • Spitale A.
        • Faquin W.C.
        • et al.
        The bethesda system for reporting thyroid cytopathology: a meta-analysis.
        Acta Cytol. 2012; 56: 333-339
        • Nishino M.
        • Krane J.F.
        Role of ancillary techniques in thyroid cytology specimens.
        Acta Cytol. 2020; 64: 40-51
        • Nishino M.
        • Nikiforova M.
        Update on molecular testing for cytologically indeterminate thyroid nodules.
        Arch Pathol Lab Med. 2018; 142: 446-457
        • Kim S.J.
        • Roh J.
        • Baek J.H.
        • et al.
        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. 2017; 28: 65-73
        • Ho A.S.
        • Sarti E.E.
        • Jain K.S.
        • et al.
        Malignancy rate in thyroid nodules classified as Bethesda category III (AUS/FLUS).
        Thyroid. 2014; 24: 832-839
        • VanderLaan P.A.
        • Marqusee E.
        • Krane J.F.
        Usefulness of diagnostic qualifiers for thyroid fine-needle aspirations with atypia of undetermined significance.
        Am J Clin Pathol. 2011; 136: 572-577
        • Vuong H.G.
        • Nguyen T.P.X.
        • Hassell L.A.
        • et al.
        Diagnostic performances of the afirma gene sequencing classifier in comparison with the gene expression classifier: a meta-analysis.
        Cancer Cytopathol. 2021; 129: 182-189
        • Domingo R.P.
        • Ogden L.L.
        • Been L.C.
        • et al.
        Identification of parathyroid tissue in thyroid fine-needle aspiration: A combined approach using cytology, immunohistochemical, and molecular methods.
        Diagn Cytopathol. 2017; 45: 526-532
        • Absher K.J.
        • Truong L.D.
        • Khurana K.K.
        • et al.
        Parathyroid cytology: avoiding diagnostic pitfalls.
        Head Neck. 2002; 24: 157-164
        • Shi Y.
        • Brandler T.C.
        • Yee-Chang M.
        • et al.
        Application of GATA 3 and TTF-1 in differentiating parathyroid and thyroid nodules on cytology specimens.
        Diagn Cytopathol. 2020; 48: 128-137
        • Trimboli P.
        • D'Aurizio F.
        • Tozzoli R.
        • et al.
        Measurement of thyroglobulin, calcitonin, and PTH in FNA washout fluids.
        Clin Chem Lab Med. 2017; 55: 914-925
        • Steen S.
        • Hysek M.
        • Zedenius J.
        • et al.
        Cyto-morphological features of parathyroid lesions: Fine-needle aspiration cytology series from an endocrine tumor referral center.
        Diagn Cytopathol. 2022; 50: 75-83
        • Cho M.
        • Oweity T.
        • Brandler T.C.
        • et al.
        Distinguishing parathyroid and thyroid lesions on ultrasound-guided fine-needle aspiration: A correlation of clinical data, ancillary studies, and molecular analysis.
        Cancer Cytopathol. 2017; 125: 674-682
        • Pusztaszeri M.P.
        • Bongiovanni M.
        • Faquin W.C.
        Update on the cytologic and molecular features of medullary thyroid carcinoma.
        Adv Anat Pathol. 2014; 21: 26-35
        • Kaushal S.
        • Iyer V.K.
        • Mathur S.R.
        • et al.
        Fine needle aspiration cytology of medullary carcinoma of the thyroid with a focus on rare variants: a review of 78 cases.
        Cytopathology. 2011; 22: 95-105
        • Papaparaskeva K.
        • Nagel H.
        • Droese M.
        Cytologic diagnosis of medullary carcinoma of the thyroid gland.
        Diagn Cytopathol. 2000; 22: 351-358
        • Suzuki A.
        • Hirokawa M.
        • Takada N.
        • et al.
        Fine-needle aspiration cytology for medullary thyroid carcinoma: a single institutional experience in Japan.
        Endocr J. 2017; 64: 1099-1104
        • Maleki Z.
        • Abram M.
        • Dell'Aquila M.
        • et al.
        Insulinoma-associated protein 1 (INSM-1) expression in medullary thyroid carcinoma FNA: a multi-institutional study.
        J Am Soc Cytopathol. 2020; 9: 185-190
        • Adel Hakim S.
        • Mohamed Abd Raboh N.
        The diagnostic utility of INSM1 and GATA3 in discriminating problematic medullary thyroid carcinoma, thyroid and parathyroid lesions.
        Pol J Pathol. 2021; 72: 11-22
        • de Micco C.
        • Chapel F.
        • Dor A.M.
        • et al.
        Thyroglobulin in medullary thyroid carcinoma: immunohistochemical study with polyclonal and monoclonal antibodies.
        Hum Pathol. 1993; 24: 256-262
        • Trimboli P.
        • Cremonini N.
        • Ceriani L.
        • et al.
        Calcitonin measurement in aspiration needle washout fluids has higher sensitivity than cytology in detecting medullary thyroid cancer: a retrospective multicentre study.
        Clin Endocrinol (Oxf). 2014; 80: 135-140
        • Nikiforova M.N.
        • Wald A.I.
        • Roy S.
        • et al.
        Targeted next-generation sequencing panel (ThyroSeq) for detection of mutations in thyroid cancer.
        J Clin Endocrinol Metab. 2013; 98: E1852-E1860
        • Nikiforov Y.E.
        • Carty S.E.
        • Chiosea S.I.
        • et al.
        Impact of the multi-gene thyroseq next-generation sequencing assay on cancer diagnosis in thyroid nodules with atypia of undetermined significance/follicular lesion of undetermined significance cytology.
        Thyroid. 2015; 25: 1217-1223
        • Camacho C.P.
        • Lindsey S.C.
        • Melo M.C.
        • et al.
        Measurement of calcitonin and calcitonin gene-related peptide mRNA refines the management of patients with medullary thyroid cancer and may replace calcitonin-stimulation tests.
        Thyroid. 2013; 23: 308-316
        • Podany P.
        • Gilani S.M.
        Hyalinizing trabecular tumor: cytologic, histologic and molecular features and diagnostic considerations.
        Ann Diagn Pathol. 2021; 54: 151803
        • Nikiforova M.N.
        • Nikiforov Y.E.
        • Ohori N.P.
        GLIS rearrangements in thyroid nodules: a key to preoperative diagnosis of hyalinizing trabecular tumor.
        Cancer Cytopathol. 2019; 127: 560-566
        • Bongiovanni M.
        • Sykiotis G.P.
        • La Rosa S.
        • et al.
        Macrofollicular variant of follicular thyroid carcinoma: a rare underappreciated pitfall in the diagnosis of thyroid carcinoma.
        Thyroid. 2020; 30: 72-80
        • Cancer Genome Atlas Research N.
        Integrated genomic characterization of papillary thyroid carcinoma.
        Cell. 2014; 159: 676-690
        • Chin P.D.
        • Zhu C.Y.
        • Sajed D.P.
        • et al.
        Correlation of thyroseq results with surgical histopathology in cytologically indeterminate thyroid nodules.
        Endocr Pathol. 2020; 31: 377-384
        • Liu R.
        • Xing M.
        TERT promoter mutations in thyroid cancer.
        Endocr Relat Cancer. 2016; 23: R143-R155
        • Song Y.S.
        • Park Y.J.
        Genomic characterization of differentiated thyroid carcinoma.
        Endocrinol Metab (Seoul). 2019; 34: 1-10
        • Ohori N.P.
        A decade into thyroid molecular testing: where do we stand?.
        J Am Soc Cytopathol. 2022; 11: 59-61
        • Chen T.
        • Gilfix B.M.
        • Rivera J.
        • et al.
        The role of the thyroSeq v3 molecular test in the surgical management of thyroid nodules in the canadian public health care setting.
        Thyroid. 2020; 30: 1280-1287
        • Nikiforov Y.E.
        • Carty S.E.
        • Chiosea S.I.
        • et al.
        Highly accurate diagnosis of cancer in thyroid nodules with follicular neoplasm/suspicious for a follicular neoplasm cytology by ThyroSeq v2 next-generation sequencing assay.
        Cancer. 2014; 120: 3627-3634
        • Zhang L.
        • Smola B.
        • Lew M.
        • et al.
        Performance of Afirma genomic sequencing classifier vs gene expression classifier in Bethesda category III thyroid nodules: an institutional experience.
        Diagn Cytopathol. 2021; 49: 921-927
        • Patel K.N.
        • Angell T.E.
        • Babiarz J.
        • et al.
        Performance of a genomic sequencing classifier for the preoperative diagnosis of cytologically indeterminate thyroid nodules.
        JAMA Surg. 2018; 153: 817-824
        • Krane J.F.
        • Cibas E.S.
        • Endo M.
        • et al.
        The Afirma Xpression Atlas for thyroid nodules and thyroid cancer metastases: Insights to inform clinical decision-making from a fine-needle aspiration sample.
        Cancer Cytopathol. 2020; 128: 452-459
        • Kaya C.
        • Dorsaint P.
        • Mercurio S.
        • et al.
        Limitations of detecting genetic variants from the RNA sequencing data in tissue and fine-needle aspiration samples.
        Thyroid. 2021; 31: 589-595
        • Sistrunk J.W.
        • Shifrin A.
        • Frager M.
        • et al.
        Clinical performance of multiplatform mutation panel and microRNA risk classifier in indeterminate thyroid nodules.
        J Am Soc Cytopathol. 2020; 9: 232-241
        • Silaghi C.A.
        • Lozovanu V.
        • Georgescu C.E.
        • et al.
        Thyroseq v3, Afirma GSC, and microRNA panels versus previous molecular tests in the preoperative diagnosis of indeterminate thyroid nodules: a systematic review and meta-analysis.
        Front Endocrinol (Lausanne). 2021; 12: 649522
        • Lupo M.A.
        • Walts A.E.
        • Sistrunk J.W.
        • et al.
        Multiplatform molecular test performance in indeterminate thyroid nodules.
        Diagn Cytopathol. 2020; 48: 1254-1264
        • Chu Y.H.
        • Sadow P.M.
        Kinase fusion-related thyroid carcinomas: distinct pathologic entities with evolving diagnostic implications.
        Diagn Histopathol (Oxf). 2021; 27: 252-262
        • Chu Y.H.
        • Wirth L.J.
        • Farahani A.A.
        • et al.
        Clinicopathologic features of kinase fusion-related thyroid carcinomas: an integrative analysis with molecular characterization.
        Mod Pathol. 2020; 33: 2458-2472
        • Chu Y.H.
        • Dias-Santagata D.
        • Farahani A.A.
        • et al.
        Clinicopathologic and molecular characterization of NTRK-rearranged thyroid carcinoma (NRTC).
        Mod Pathol. 2020; 33: 2186-2197
        • Molinaro E.
        • Romei C.
        • Biagini A.
        • et al.
        Anaplastic thyroid carcinoma: from clinicopathology to genetics and advanced therapies.
        Nat Rev Endocrinol. 2017; 13: 644-660
        • Baloch Z.W.
        • Asa S.L.
        • Barletta J.A.
        • et al.
        Overview of the 2022 WHO classification of thyroid neoplasms.
        Endocr Pathol. 2022; 33: 27-63
        • Wiseman S.M.
        • Loree T.R.
        • Rigual N.R.
        • et al.
        Anaplastic transformation of thyroid cancer: review of clinical, pathologic, and molecular evidence provides new insights into disease biology and future therapy.
        Head Neck. 2003; 25: 662-670
        • McIver B.
        • Hay I.D.
        • Giuffrida D.F.
        • et al.
        Anaplastic thyroid carcinoma: a 50-year experience at a single institution.
        Surgery. 2001; 130: 1028-1034
        • Venkatesh Y.S.
        • Ordonez N.G.
        • Schultz P.N.
        • et al.
        Anaplastic carcinoma of the thyroid. A clinicopathologic study of 121 cases.
        Cancer. 1990; 66: 321-330
        • Smallridge R.C.
        • Ain K.B.
        • Asa S.L.
        • et al.
        American Thyroid Association guidelines for management of patients with anaplastic thyroid cancer.
        Thyroid. 2012; 22: 1104-1139
        • Ohori N.P.
        • Landau M.S.
        • Manroa P.
        • et al.
        Molecular-derived estimation of risk of malignancy for indeterminate thyroid cytology diagnoses.
        J Am Soc Cytopathol. 2020; 9: 213-220
        • Gajzer D.C.
        • Tjendra Y.
        • Kerr D.A.
        • et al.
        Probability of malignancy as determined by thyroSeq v3 genomic classifier varies according to the subtype of atypia.
        Cancer Cytopathol. 2022; (In press)https://doi.org/10.1002/cncy.22617
        • Parker K.G.
        • White M.G.
        • Cipriani N.A.
        Comparison of molecular methods and BRAF immunohistochemistry (VE1 Clone) for the detection of BRAF V600E mutation in papillary thyroid carcinoma: a meta-analysis.
        Head Neck Pathol. 2020; 14: 1067-1079
        • Oishi N.
        • Kondo T.
        • Vuong H.G.
        • et al.
        Immunohistochemical detection of NRAS(Q61R) protein in follicular-patterned thyroid tumors.
        Hum Pathol. 2016; 53: 51-57
        • Lee Y.C.
        • Chen J.Y.
        • Huang C.J.
        • et al.
        Detection of NTRK1/3 rearrangements in papillary thyroid carcinoma using immunohistochemistry, fluorescent in situ hybridization, and next-generation sequencing.
        Endocr Pathol. 2020; 31: 348-358
        • Cracolici V.
        • Ritterhouse L.L.
        • Segal J.P.
        • et al.
        Follicular thyroid neoplasms: comparison of clinicopathologic and molecular features of atypical adenomas and follicular thyroid carcinomas.
        Am J Surg Pathol. 2020; 44: 881-892
        • Derwahl M.
        • Studer H.
        Hyperplasia versus adenoma in endocrine tissues: are they different?.
        Trends Endocrinol Metab. 2002; 13: 23-28
        • Harrer P.
        • Brocker M.
        • Zint A.
        • et al.
        The clonality of nodules in recurrent goiters at second surgery.
        Langenbecks Arch Surg. 1998; 383: 453-455
        • Apel R.L.
        • Ezzat S.
        • Bapat B.V.
        • et al.
        Clonality of thyroid nodules in sporadic goiter.
        Diagn Mol Pathol. 1995; 4: 113-121