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Paja M, Del Cura JL, Zabala R, Korta I, Gutiérrez MT, Expósito A, Ugalde A. A simplified four-tier classification for thyroid core needle biopsy. J Endocrinol Invest 2025; 48:895-904. [PMID: 39576555 DOI: 10.1007/s40618-024-02508-x] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 05/26/2024] [Accepted: 11/17/2024] [Indexed: 03/28/2025]
Abstract
PURPOSE To propose a simplified histological classification for core-needle biopsy (CNB) of thyroid nodules with four diagnostic categories (DC) and provide the risk of malignancy (ROM) and the expected incidence for each DC. There is no uniform scheme for categorizing CNB specimens, except for a Korean diagnostic classification similar to the Bethesda system for FNAC. METHODS Data from a single institution using CNB as a routine diagnostic tool for thyroid nodules. Biopsies were classified as non-diagnostic, benign, follicular tumour (FT) or malignant. The frequency of each DC and the correlation with surgical pathology of nodules undergoing surgery after CNB were evaluated. RESULTS Of 6284 CNBs on 5782 nodules [195 (3.1%) non-diagnostic, 5043 (80.3%) benign, 435 (6.9%) FT and 611 (9.7%) malignant], 1914 nodules (33.1%) underwent surgery after 2016 CNBs: 48 non-diagnostic, 1035 benign, 355 FT and 578 malignant. Malignancy was diagnosed after surgery in 11 non-diagnostic (ROM: 22.9%), 23 benign (ROM: 2.2%), 44 FT (ROM: 12.4%, 11.5% excluding low-grade malignancy) and 568 malignant CNBs (ROM: 98.3%, 93.8% excluding low-grade malignancy). Sensitivity and positive predictive value for malignancy of FT or malignant CNB were 94.7% and 65.6%, and for thyroid neoplasm (adenoma or carcinoma) were 93.2% and 92.6%. CONCLUSIONS Our diagnostic classification for CNB of thyroid nodules has a high diagnostic accuracy with a low rate of indeterminate categories. This classification, applied in a Western practice, shows a low ROM for nodules classified as follicular tumours, which could be improved with immunohistochemical studies.
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Affiliation(s)
- M Paja
- Endocrinology Department, Hospital Universitario Basurto, OSI Bilbao-Basurto, Bilbao, Spain.
- University of the Basque Country, UPV/EHU, Leioa, Spain.
| | - J L Del Cura
- University of the Basque Country, UPV/EHU, Leioa, Spain
- Radiology Department, Hospital Universitario Donostia, Donostia, Spain
| | - R Zabala
- Radiology Department, Hospital Universitario Basurto, OSI Bilbao-Basurto, Bilbao, Spain
| | - I Korta
- University of the Basque Country, UPV/EHU, Leioa, Spain
- Radiology Department, Hospital Universitario Basurto, OSI Bilbao-Basurto, Bilbao, Spain
| | - Mª T Gutiérrez
- University of the Basque Country, UPV/EHU, Leioa, Spain
- Endocrine Surgery Department, Hospital Universitario Basurto, OSI Bilbao-Basurto, Bilbao, Spain
| | - A Expósito
- University of the Basque Country, UPV/EHU, Leioa, Spain
- Endocrine Surgery Department, Hospital Universitario Basurto, OSI Bilbao-Basurto, Bilbao, Spain
| | - A Ugalde
- Pathology Department, Hospital Universitario Basurto, OSI Bilbao-Basurto, Bilbao, Spain
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Taydas O, Arik E, Sevinc OF, Kara AB, Ozdemir M, Cengiz H, Bayhan Z, Ozturk MH. Current role of interventional radiology in thyroid nodules. Front Endocrinol (Lausanne) 2024; 15:1405705. [PMID: 39355619 PMCID: PMC11442250 DOI: 10.3389/fendo.2024.1405705] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Figures] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 03/23/2024] [Accepted: 09/02/2024] [Indexed: 10/03/2024] Open
Abstract
Thyroid nodules are a prevalent health issue in society. Interventional radiological methods are successfully applied for both the diagnosis and treatment of nodules. Diagnostically, a fine-needle aspiration biopsy and a core needle biopsy can be performed to ascertain the benign or malignant nature of a lesion. In recent years, imaging-guided percutaneous treatment methods have become popular in the treatment of thyroid nodules. Aspiration, ablation, and embolization are techniques employed in the treatment process. In this study, we aimed to discuss the current role of interventional radiology in the diagnosis and treatment of thyroid nodules, which occupy an important place in clinical practice.
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Affiliation(s)
- Onur Taydas
- Department of Radiology, Faculty of Medicine, Sakarya University, Sakarya, Türkiye
| | - Erbil Arik
- Department of Radiology, Faculty of Medicine, Marmara University, İstanbul, Türkiye
| | | | - Ahmet Burak Kara
- Department of Radiology, Gaziantep City Hospital, Gaziantep, Türkiye
| | - Mustafa Ozdemir
- Department of Radiology, Faculty of Medicine, Sakarya University, Sakarya, Türkiye
| | - Hasret Cengiz
- Department of Endocrinology and Metabolism, Faculty of Medicine, Sakarya University, Sakarya, Türkiye
| | - Zulfu Bayhan
- Department of General Surgery, Faculty of Medicine, Sakarya University, Sakarya, Türkiye
| | - Mehmet Halil Ozturk
- Department of Radiology, Faculty of Medicine, Sakarya University, Sakarya, Türkiye
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3
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Xia Z, Huang X, Zhang T, Gao Z, Tang X, Zhang W, Miao Q. Ultrasonographic features and diagnostic accuracy of FNA and CNB in secondary thyroid malignancies: A retrospective study. Heliyon 2024; 10:e36305. [PMID: 39224267 PMCID: PMC11367495 DOI: 10.1016/j.heliyon.2024.e36305] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 11/09/2023] [Revised: 08/05/2024] [Accepted: 08/13/2024] [Indexed: 09/04/2024] Open
Abstract
Objective This study aims to examine the ultrasonographic features of secondary thyroid malignancies and compare the diagnostic efficacy of fine-needle aspiration (FNA) and core needle biopsy (CNB) in this condition. Methods A retrospective analysis was conducted on 29 patients with secondary thyroid malignancies treated at our center between July 2011 and October 2022. Ultrasound images and clinical data were analyzed, and the lesions were classified according to the American College of Radiology Thyroid Imaging Reporting and Data System (ACR TI-RADS). Results Among the 29 patients studied, primary tumor sites were predominantly the esophagus, lung, and nasopharynx. Comprehensive ultrasound data was available for 28 of these patients, revealing nodular lesions in 24 cases and diffuse lesions in 4 cases. Nodular lesions were predominantly solid or nearly solid hypoechoic nodules with parallel growth and extrathyroidal extension features, with a few showing macrocalcifications. Most patients had varying degrees of metastasis to neck lymph nodes. FNA accurately diagnosed 31.6 % of the lesions as secondary thyroid malignancies, while 5.3 % were misdiagnosed as papillary thyroid carcinoma (PTC). However, CNB demonstrated 100 % reliability in diagnosing secondary thyroid malignancies. Conclusion This study's categorization of secondary thyroid malignancy ultrasonographic features identifies nodular and diffuse patterns, with the application of ACR TI-RADS proving effective for nodular types. In detecting these lesions, CNB demonstrates superior sensitivity compared to FNA. Thus, in cases of thyroid lesions suspected to be malignant, particularly with enlarged neck lymph nodes and in patients with a history of malignancy, CNB is recommended as the diagnostic method of choice.
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Affiliation(s)
- Zhen Xia
- Department of Ultrasound, Jiangsu Cancer Hospital & Jiangsu Institute of Cancer Research & The Affiliated Cancer Hospital of Nanjing Medical University, Nanjing, China
| | - Xiaochen Huang
- Department of Pathology, Jiangsu Cancer Hospital & Jiangsu Institute of Cancer Research & The Affiliated Cancer Hospital of Nanjing Medical University, Nanjing, China
| | - Ting Zhang
- Department of Ultrasound, Jiangsu Cancer Hospital & Jiangsu Institute of Cancer Research & The Affiliated Cancer Hospital of Nanjing Medical University, Nanjing, China
| | - Zhigang Gao
- Department of Ultrasound, Jiangsu Cancer Hospital & Jiangsu Institute of Cancer Research & The Affiliated Cancer Hospital of Nanjing Medical University, Nanjing, China
| | - Xiuliang Tang
- Department of Ultrasound, Jiangsu Cancer Hospital & Jiangsu Institute of Cancer Research & The Affiliated Cancer Hospital of Nanjing Medical University, Nanjing, China
| | - Wei Zhang
- Department of Ultrasound, Jiangsu Cancer Hospital & Jiangsu Institute of Cancer Research & The Affiliated Cancer Hospital of Nanjing Medical University, Nanjing, China
| | - Qing Miao
- Department of Ultrasound, Jiangsu Cancer Hospital & Jiangsu Institute of Cancer Research & The Affiliated Cancer Hospital of Nanjing Medical University, Nanjing, China
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4
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Dolidze DD, Covantsev S, Chechenin GM, Pichugina NV, Bedina AV, Bumbu A. Core needle biopsy for thyroid nodules assessment-a new horizon? World J Clin Oncol 2024; 15:580-586. [PMID: 38835840 PMCID: PMC11145964 DOI: 10.5306/wjco.v15.i5.580] [Citation(s) in RCA: 3] [Impact Index Per Article: 3.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 12/03/2023] [Revised: 01/29/2024] [Accepted: 04/10/2024] [Indexed: 05/21/2024] Open
Abstract
Ultrasound-guided fine-needle aspiration is the standard for evaluating thyroid nodules with a high safety profile and a relatively low number of non-diagnostic cytological findings. Nevertheless, this diagnostic method traditionally has its weak points. Several diagnostic categories such as Bethesda I, III and IV are not reliable for thyroid carcinoma risk assessment. Recent advancements in a core needle biopsy made it possible to use this tool as a new method for thyroid nodules evaluation. The main feature of this method is the use of thin needles (18-21G) and guns with an automatic trigger mechanism. The histological material collected with the use of a core needle biopsy is usually superior to cytological. Therefore, the core needle biopsy can be used as a complementary technique to a standard fine needle aspiration in difficult and dubious cases of thyroid neoplasia with uncertain malignant potential.
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Affiliation(s)
- David D Dolidze
- Department of Clinical Research and Development, Botkin Hospital, Moscow 125284, Russia
- Department of Surgery, Russian Medical Academy of Continuous Professional Education, Moscow 125445, Russia
| | - Serghei Covantsev
- Department of Clinical Research and Development, Botkin Hospital, Moscow 125284, Russia
- Emergency Surgery №76, Botkin Hospital, Moscow 125284, Russia
| | - Grigorii M Chechenin
- Department of Surgery, Russian Medical Academy of Continuous Professional Education, Moscow 125445, Russia
- Department of Surgery, Botkin Hospital, Moscow 125284, Russia
| | - Natalia V Pichugina
- Department of Medical Ultrasonography, Botkin Hospital, Moscow 125284, Russia
| | - Anastasia V Bedina
- Medicine, Moscow State Medical University I.M. Sechenov, Moscow 119048, Russia
| | - Anna Bumbu
- Department of Oncology, Botkin Hospital, Moscow 125284, Russia
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Moon HH, Chung SR, Choi YJ, Sung TY, Song DE, Kim TY, Lee JH, Baek JH. The Diagnostic Role of Repeated Biopsy of Thyroid Nodules with Atypia of Undetermined Significance with Architectural Atypia on Core-Needle Biopsy. Endocrinol Metab (Seoul) 2024; 39:300-309. [PMID: 38171211 PMCID: PMC11066445 DOI: 10.3803/enm.2023.1818] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 09/04/2023] [Revised: 10/26/2023] [Accepted: 11/14/2023] [Indexed: 01/05/2024] Open
Abstract
BACKGRUOUND We aimed to evaluate the utility of repeat biopsy of thyroid nodules classified as atypia of undetermined significance with architectural atypia (IIIB) on core-needle biopsy (CNB). METHODS This retrospective study evaluated patients with thyroid nodules categorized as IIIB on CNB between 2013 and 2015. Demographic characteristics, subsequent biopsy results, and ultrasound (US) images were evaluated. The malignancy rates of nodules according to number of CNBs and the number of IIIB diagnoses was compared. Demographic and US features were evaluated to determine factors predictive of malignancy. RESULTS Of 1,003 IIIB nodules on CNB, the final diagnosis was determined for 328 (32.7%) nodules, with 121 of them confirmed as malignant, resulting in a malignancy rate of 36.9% (95% confidence interval, 31.7% to 42.1%). Repeat CNB was performed in 248 nodules (24.7%), with 75 (30.2%), 131 (52.8%), 13 (5.2%), 26 (10.5%), one (0.4%), and two (0.8%) reclassified into categories II, IIIB, IIIA, IV, V, and VI, respectively. Malignancy rates were not significantly affected by the number of CNBs (P=0.291) or the number of IIIB diagnoses (P=0.473). None of the nodules confirmed as category II on repeat CNB was malignant. US features significantly associated with malignancy (P<0.003) included solid composition, irregular margins, microcalcifications, and high suspicion on the US risk stratification system. CONCLUSION Repeat biopsy of nodules diagnosed with IIIB on CNB did not increase the detection of malignancy but can potentially reduce unnecessary surgery. Repeat biopsy should be performed selectively, with US features guiding the choice between repeat biopsy and diagnostic surgery.
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Affiliation(s)
- Hye Hyeon Moon
- Department of Radiology and Research Institute of Radiology, Asan Medical Center, University of Ulsan College of Medicine, Seoul, Korea
| | - Sae Rom Chung
- Department of Radiology and Research Institute of Radiology, Asan Medical Center, University of Ulsan College of Medicine, Seoul, Korea
| | - Young Jun Choi
- Department of Radiology and Research Institute of Radiology, Asan Medical Center, University of Ulsan College of Medicine, Seoul, Korea
| | - Tae-Yon Sung
- Department of Surgery, Asan Medical Center, University of Ulsan College of Medicine, Seoul, Korea
| | - Dong Eun Song
- Department of Pathology, Asan Medical Center, University of Ulsan College of Medicine, Seoul, Korea
| | - Tae Yong Kim
- Department of Internal Medicine, Asan Medical Center, University of Ulsan College of Medicine, Seoul, Korea
| | - Jeong Hyun Lee
- Department of Radiology and Research Institute of Radiology, Asan Medical Center, University of Ulsan College of Medicine, Seoul, Korea
| | - Jung Hwan Baek
- Department of Radiology and Research Institute of Radiology, Asan Medical Center, University of Ulsan College of Medicine, Seoul, Korea
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Sgrò D, Brancatella A, Greco G, Torregrossa L, Piaggi P, Viola N, Rago T, Basolo F, Giannini R, Materazzi G, Elisei R, Santini F, Latrofa F. Cytological and Ultrasound Features of Thyroid Nodules Correlate With Histotypes and Variants of Thyroid Carcinoma. J Clin Endocrinol Metab 2023; 108:e1186-e1192. [PMID: 37265229 DOI: 10.1210/clinem/dgad313] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.5] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 02/05/2023] [Revised: 05/04/2023] [Accepted: 05/30/2023] [Indexed: 06/03/2023]
Abstract
CONTEXT Prognosis is excellent for papillary thyroid carcinoma (PTC), noninvasive follicular thyroid neoplasia with papillary-like nuclear features (NIFT-P), and follicular thyroid carcinoma (FTC) but is poor for poorly differentiated thyroid carcinoma (PDTC) and anaplastic thyroid carcinoma (ATC). Among PTCs, the prognosis is more favorable for follicular (FV-PTC) and classic (CV-PTC) than for tall cell (TCV-PTC), and solid (SV-PTC) variants. OBJECTIVE To associate histotypes and variants of thyroid carcinoma with ultrasound and cytological features. METHODS Histology of 1018 benign tumors and 514 PTC (249 CV, 167 FV, 49 TC, 34 SV, and 15 other variants), 52 NIFT-P, 50 FTC, 11 PDTC, and 3 ATC was correlated with fine-needle aspiration biopsy categories (Italian classification: TIR1, TIR2, TIR3A, TIR3B, TIR4, and TIR5) and ultrasound features at the Endocrinology Unit, University Hospital of Pisa. In total, 1117 patients with thyroid nodule(s) who underwent thyroidectomy were included. RESULTS Of PTC, 36.3% had indeterminate cytology (TIR3A or TIR3B), 56.6% were suspicious for malignancy or malignant (TIR4 or TIR5); 84.0% FTC and 69.3% NIFT-P were TIR3A or TIR3B; 72.5% FV-PTC and 73.6% SV-PTC were TIR3A or TIR3B; 79.9% CV-PTC and 95.9% TCV-PTC were TIR4 or TIR5. The association of a hypoechoic pattern, irregular margins, and no microcalcifications was more frequent in TCV-PTC than in CV-PTC (P = .02, positive predictive value = 38.9%; negative predictive value = 85.5%). CONCLUSION At cytology, most FTC, NIFT-P, FV-PTC, and SV-PTC were indeterminate, most CV-PTC and TCV-PTC were suspicious for malignancy or malignant. Ultrasound can be helpful in ruling out TCV-PTC.
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Affiliation(s)
- Daniele Sgrò
- Endocrinology Unit, Department of Clinical and Experimental Medicine, University of Pisa, Pisa, Italy
| | - Alessandro Brancatella
- Endocrinology Unit, Department of Clinical and Experimental Medicine, University of Pisa, Pisa, Italy
| | - Giuseppe Greco
- Endocrinology Unit, Department of Clinical and Experimental Medicine, University of Pisa, Pisa, Italy
| | - Liborio Torregrossa
- Pathology Unit, Department of Surgical, Medical and Molecular Pathology and Critical Area, University of Pisa, Pisa, Italy
| | - Paolo Piaggi
- Endocrinology Unit, Department of Clinical and Experimental Medicine, University of Pisa, Pisa, Italy
| | - Nicola Viola
- Endocrinology Unit, Department of Clinical and Experimental Medicine, University of Pisa, Pisa, Italy
| | - Teresa Rago
- Endocrinology Unit, Department of Clinical and Experimental Medicine, University of Pisa, Pisa, Italy
| | - Fulvio Basolo
- Pathology Unit, Department of Surgical, Medical and Molecular Pathology and Critical Area, University of Pisa, Pisa, Italy
| | - Riccardo Giannini
- Pathology Unit, Department of Surgical, Medical and Molecular Pathology and Critical Area, University of Pisa, Pisa, Italy
| | - Gabriele Materazzi
- Unit of Endocrine Surgery, Department of Surgical, Medical and Molecular Pathology and Critical Area, University of Pisa, Pisa, Italy
| | - Rossella Elisei
- Endocrinology Unit, Department of Clinical and Experimental Medicine, University of Pisa, Pisa, Italy
| | - Ferruccio Santini
- Endocrinology Unit, Department of Clinical and Experimental Medicine, University of Pisa, Pisa, Italy
| | - Francesco Latrofa
- Endocrinology Unit, Department of Clinical and Experimental Medicine, University of Pisa, Pisa, Italy
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Durante C, Hegedüs L, Czarniecka A, Paschke R, Russ G, Schmitt F, Soares P, Solymosi T, Papini E. 2023 European Thyroid Association Clinical Practice Guidelines for thyroid nodule management. Eur Thyroid J 2023; 12:e230067. [PMID: 37358008 PMCID: PMC10448590 DOI: 10.1530/etj-23-0067] [Citation(s) in RCA: 128] [Impact Index Per Article: 64.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 04/04/2023] [Accepted: 06/23/2023] [Indexed: 06/27/2023] Open
Abstract
With the widespread use of sensitive imaging techniques, which include neck visualization, a conspicuous number of thyroid nodules emerge and demand attention. Most lesions are benign, asymptomatic, and do not warrant treatment. In the case of cancer diagnosis, most are small, intrathyroidal and indolent neoplasms that can safely be managed conservatively. There is a pronounced need for more cost-effective, risk-adapted approaches to the management of this highly prevalent condition, taking the wishes of the patient into consideration. Thus, the present guidelines aim at providing a clinical practice guide for the initial workup and the subsequent management of adult individuals harboring thyroid nodules. Importantly, these guidelines are not intended to cover the management of thyroid malignancy. The manuscript and the specific recommendations were developed by reconciling the best available research evidence with the knowledge and clinical experience of the panelists and updating aspects of a number of previous European Thyroid Association guidelines.
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Affiliation(s)
- Cosimo Durante
- Department of Translational and Precision Medicine, Sapienza University of Rome, Rome, Italy
| | - Laszlo Hegedüs
- Department of Endocrinology, Odense University Hospital, Odense, Denmark
| | - Agnieszka Czarniecka
- M. Sklodowska-Curie National Research, Institute of Oncology Gliwice Branch, Gliwice, Poland
| | - Ralf Paschke
- Cumming School of Medicine, University of Calgary, Calgary, Alberta, Canada
| | - Gilles Russ
- Thyroid and Endocrine Tumors Department, Pitié-Salpêtrière Hospital, Sorbonne University GRC N°16, Paris, France
| | - Fernando Schmitt
- Faculty of Medicine of University of Porto, CINTESIS@RISE and Institute of Molecular Pathology and Immunology, University of Porto (Ipatimup), Porto, Portugal
| | - Paula Soares
- Institute of Investigation and Innovation in Health (I3S), Faculty of Medicine of the University of Porto, Porto, Portugal
| | - Tamas Solymosi
- Endocrinology and Metabolism Clinic, Bugat Hospital, Gyöngyös, Hungary
| | - Enrico Papini
- Department of Endocrine and Metabolic Diseases, Regina Apostolorum Hospital, Albano, Rome, Italy
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Jung CK. Reevaluating diagnostic categories and associated malignancy risks in thyroid core needle biopsy. J Pathol Transl Med 2023; 57:208-216. [PMID: 37460395 PMCID: PMC10369141 DOI: 10.4132/jptm.2023.06.20] [Citation(s) in RCA: 5] [Impact Index Per Article: 2.5] [Reference Citation Analysis] [Abstract] [Key Words] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/11/2023] [Accepted: 06/19/2023] [Indexed: 07/28/2023] Open
Abstract
As the application of core needle biopsy (CNB) in evaluating thyroid nodules rises in clinical practice, the 2023 Korean Thyroid Association Management Guidelines for Patients with Thyroid Nodules have officially recognized its value for the first time. CNB procures tissue samples preserving both histologic structure and cytologic detail, thereby supplying substantial material for an accurate diagnosis and reducing the necessity for repeated biopsies or subsequent surgical interventions. The current review introduces the risk of malignancy within distinct diagnostic categories, emphasizing the implications of noninvasive follicular thyroid neoplasm with papillary-like nuclear features on these malignancy risks. Prior research has indicated diagnostic challenges associated with follicular-patterned lesions, resulting in notable variation within indeterminate diagnostic categories. The utilization of mutation-specific immunostaining in CNB enhances the accuracy of lesion classification. This review underlines the essential role of a multidisciplinary approach in diagnosing follicular-patterned lesions and the potential of mutation-specific immunostaining to strengthen diagnostic consensus and inform patient management decisions.
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Affiliation(s)
- Chan Kwon Jung
- Department of Hospital Pathology, College of Medicine, The Catholic University of Korea, Seoul, Korea
- Cancer Research Institute, College of Medicine, The Catholic University of Korea, Seoul, Korea
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9
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Kim M, Jeon S, Jung CK. Preoperative Risk Stratification of Follicular-patterned Thyroid Lesions on Core Needle Biopsy by Histologic Subtyping and RAS Variant-specific Immunohistochemistry. Endocr Pathol 2023:10.1007/s12022-023-09763-3. [PMID: 37040004 DOI: 10.1007/s12022-023-09763-3] [Citation(s) in RCA: 6] [Impact Index Per Article: 3.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Accepted: 03/29/2023] [Indexed: 04/12/2023]
Abstract
Follicular-patterned lesions often have indeterminate results (diagnostic category III or IV) by core needle biopsy (CNB) and fine needle aspiration (FNA). However, CNB diagnoses follicular neoplasm (category IV) more frequently than FNA. Therefore, we aimed to develop a risk stratification system for CNB samples with category III/IV using immunohistochemistry (IHC). The specificity of the RAS Q61R antibody was validated on 58 thyroid nodules with six different types of RAS genetic variants and 40 cases of RAS wild-type. We then applied IHC analysis of RAS Q61R to 207 CNB samples with category III/IV in which all patients underwent surgical resection. RAS Q61R IHC had 98% sensitivity and 98% specificity for detecting the RAS p.Q16R variant. In an independent dataset, the positive rate of RAS Q61R was significantly higher in NIFTP (48%) and malignancies (45%) than in benign tumors (19%). The risk of NIFTP/malignancy was highest in the group with nuclear atypia and RAS Q61R expression (86%) and lowest in the group without both parameters (32%). The high-risk group with either nuclear atypia or RAS Q61R had 67.3% sensitivity, 73.4% specificity, 75.2% positive predictive value, and 65.1% negative predictive value for identifying NIFTP/malignancy. We conclude that RAS Q61R IHC can be a rule-in diagnostic test for NIFTP/malignancy in CNB category III/IV results. Combining of the histologic parameter (nuclear atypia) with RAS Q61R IHC results can further stratify CNB category III/IV into a high-risk group, which is sufficient for a surgical referral, and a low-risk group sufficient for observation.
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Affiliation(s)
- Meejeong Kim
- Department of Pathology, Seoul St. Mary's Hospital, College of Medicine, The Catholic University of Korea, Seoul, Korea
| | - Sora Jeon
- College of Medicine, Cancer Research Institute, The Catholic University of Korea, Seoul, Korea
| | - Chan Kwon Jung
- Department of Pathology, Seoul St. Mary's Hospital, College of Medicine, The Catholic University of Korea, Seoul, Korea.
- College of Medicine, Cancer Research Institute, The Catholic University of Korea, Seoul, Korea.
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10
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Kim H, Shin JH, Kim KE, Kim MK, Oh J, Hahn SY. Subcategorization of intermediate suspicion thyroid nodules based on suspicious ultrasonographic findings. Ultrasonography 2023; 42:307-313. [PMID: 36935593 PMCID: PMC10071054 DOI: 10.14366/usg.22096] [Citation(s) in RCA: 5] [Impact Index Per Article: 2.5] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/13/2022] [Accepted: 12/22/2022] [Indexed: 02/25/2023] Open
Abstract
PURPOSE This study compared the malignancy risk of intermediate suspicion thyroid nodules according to the presence of suspicious ultrasonographic (US) findings. METHODS From January 2014 to December 2014, 299 consecutive intermediate suspicion thyroid nodules in 281 patients (mean age, 50.6±12.5 years) with final diagnoses were included in this study. Two radiologists retrospectively reviewed the US findings and subcategorized the intermediate suspicion category into nodules without suspicious findings and nodules with suspicious findings, including punctate echogenic foci, nonparallel orientation, or irregular margins. The malignancy rates were compared between the two subcategory groups. RESULTS Of the 299 intermediate suspicion thyroid nodules, 230 (76.9%) were subcategorized as nodules without suspicious findings and 69 (23.1%) as nodules with suspicious findings. The total malignancy rate was 33.4% (100/299) and the malignancy rate of nodules with suspicious findings was significantly higher than that of nodules without suspicious findings (47.8% vs. 29.1%, P=0.004). In nodules with suspicious findings, the most common suspicious finding was punctate echogenic foci (48/82, 58.5%) followed by nonparallel orientation (22/82, 26.8%) and irregular margins (12/82, 14.6%). Thirteen nodules had two suspicious findings simultaneously. A linearly increasing trend in the malignancy rate was observed according to the number of suspicious US findings (P for trend=0.001). CONCLUSION Intermediate suspicion thyroid nodules with suspicious findings showed a higher malignancy rate than those without suspicious findings. Further management guidelines for nodules with suspicious findings should differ from guidelines for nodules without suspicious findings, even in the same US category.
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Affiliation(s)
- Haejung Kim
- Department of Radiology and Center for Imaging Science, Samsung Medical Center, Sungkyunkwan University School of Medicine, Seoul, Korea
| | - Jung Hee Shin
- Department of Radiology and Center for Imaging Science, Samsung Medical Center, Sungkyunkwan University School of Medicine, Seoul, Korea
| | - Ka Eun Kim
- Department of Radiology and Center for Imaging Science, Samsung Medical Center, Sungkyunkwan University School of Medicine, Seoul, Korea
| | - Myoung Kyoung Kim
- Department of Radiology and Center for Imaging Science, Samsung Medical Center, Sungkyunkwan University School of Medicine, Seoul, Korea
| | - Jiyun Oh
- Department of Radiology and Center for Imaging Science, Samsung Medical Center, Sungkyunkwan University School of Medicine, Seoul, Korea
| | - Soo Yeon Hahn
- Department of Radiology and Center for Imaging Science, Samsung Medical Center, Sungkyunkwan University School of Medicine, Seoul, Korea
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11
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Hwang YJ, Koo HR, Park JS. Follow-up of benign thyroid nodules confirmed by ultrasound-guided core needle biopsy after inconclusive cytology on fine-needle aspiration biopsy. Ultrasonography 2023; 42:121-128. [PMID: 36588182 PMCID: PMC9816704 DOI: 10.14366/usg.22115] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/02/2022] [Accepted: 09/21/2022] [Indexed: 01/13/2023] Open
Abstract
PURPOSE The goal of this study was to follow benign thyroid nodules confirmed by ultrasound (US)-guided core needle biopsy (CNB) after inconclusive cytology on fine-needle aspiration (FNA) biopsy. METHODS Sixty-two thyroid nodules from 62 patients with CNB-confirmed benign histology that initially had inconclusive cytology on FNA were retrospectively included. The thyroid nodules were followed for 38.7 months (median, 27.5 months; range, 6 to 101 months), and the US findings of biopsied nodules, such as the interval change in size, US characteristics, and imaging category based on the Korean Thyroid Imaging Reporting and Data System (K-TIRADS), were evaluated. In addition, patients' clinical records were reviewed for any further management or newly diagnosed thyroid malignancy. RESULTS Among 62 cases, three (4.8%) showed interval size growth, while 59 (95.2%) demonstrated no interval change or a decrease in size. There was no upgrade of K-TIRADS category or any newly diagnosed malignancy during the follow-up period. CONCLUSION US-guided CNB-confirmed benign thyroid nodules with inconclusive cytology on FNA showed a stable status during follow-up, and repeated CNB could be helpful in the management of nodules with inconclusive cytology on FNA.
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Affiliation(s)
- Yoon Ji Hwang
- Department of Radiology, Hanyang University College of Medicine, Seoul, Korea
| | - Hye Ryoung Koo
- Department of Radiology, Hanyang University College of Medicine, Seoul, Korea
| | - Jeong Seon Park
- Department of Radiology, Hanyang University College of Medicine, Seoul, Korea,Correspondence to: Jeong Seon Park, PhD, Department of Radiology, Hanyang University College of Medicine, 222-1 Wangsimni-ro, Seongdong-gu, Seoul 04763, Korea Tel. +82-2-2290-9164 Fax. +82-2-2293-2111 E-mail:
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12
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Li R, Liang Z, Wang X, Chen L. Role of echogenic foci in ultrasonographic risk stratification of thyroid nodules: Echogenic focus scoring in the American College of Radiology Thyroid Imaging Reporting and Data System. Front Oncol 2022; 12:929500. [PMID: 36106124 PMCID: PMC9465029 DOI: 10.3389/fonc.2022.929500] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/17/2022] [Accepted: 08/08/2022] [Indexed: 11/21/2022] Open
Abstract
Background Although echogenic foci may raise malignancy rates in thyroid nodules, the association between peripheral calcification or macrocalcification and thyroid carcinoma is controversial. We evaluated the malignancy probability of various echogenic foci and explored whether the method of determining a thyroid nodule’s point score in the echogenic focus category of the American College of Radiology (ACR) Thyroid Imaging Reporting and Data System (TI-RADS) is reasonable. Methods We retrospectively evaluated 819 patients with 852 nodules. The patterns of echogenic foci on ultrasonography were classified into the following four categories: punctate echogenic foci, macrocalcification, peripheral calcification, and multiple different types of echogenic foci. The core needle biopsy results were divided into two groups: benign and malignant or suspicious for malignancy. Results Among the 852 nodules, 471 (55.3%) had echogenic foci on ultrasonography. Of these nodules, there was no significant statistical difference in the malignant or suspicious for malignancy rate between nodules with peripheral calcification and those with macrocalcification [40.0% (8/20) vs. 30.6% (11/36), respectively; p = 0.474]. The incidence of malignancy or suspicious for malignancy for nodules with peripheral calcification, macrocalcification, or multiple different types of echogenic foci was significantly lower than the incidence for punctate echogenic foci alone, with odds ratios of 0.265 [95% confidence interval (CI): 0.105–0.667; p = 0.005], 0.175 (95% CI: 0.083–0.368; p = 0.000), and 0.256 (95% CI: 0.136–0.482; p = 0.000), respectively. Conclusion We found no significant statistical difference in the risk of malignancy or suspicious for malignancy rate between peripheral calcification and macrocalcification in thyroid nodules. We observed that nodules with multiple different types of echogenic foci were not associated with higher malignant or suspicious for malignancy rates compared with nodules with punctate echogenic foci alone.
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13
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Kwon H, Lee J, Hong SW, Kwon HJ, Kwak JY, Yoon JH. Fine Needle Aspiration Cytology vs. Core Needle Biopsy for Thyroid Nodules: A Prospective, Experimental Study Using Surgical Specimen. TAEHAN YONGSANG UIHAKHOE CHI 2022; 83:645-657. [PMID: 36238513 PMCID: PMC9514511 DOI: 10.3348/jksr.2021.0125] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Subscribe] [Scholar Register] [Received: 07/06/2021] [Revised: 08/30/2021] [Accepted: 09/11/2021] [Indexed: 06/16/2023]
Abstract
PURPOSE To evaluate and compare the diagnostic outcomes of ultrasonography (US)-guided fine needle aspiration (FNA) and core needle biopsy (CNB) performed on the same thyroid nodule using a surgical specimen for direct comparison. MATERIALS AND METHODS We included 89 thyroid nodules from 88 patients from February 2015 to January 2016. The inclusion criterion was thyroid nodules measuring ≥ 20 mm (mean size: 40.0 ± 15.3 mm). Immediately after surgical resection, FNA and subsequent CNB were performed on the surgical specimen under US guidance. FNA and CNB cytopathologic results on the specimen were compared with the surgical diagnosis. RESULTS Among the 89 nodules, 30 were malignant and 59 were benign. Significantly higher inconclusive rates were seen in FNA for malignant than benign nodules (80.0% vs. 39.0%, p < 0.001). For CNB, conclusive and inconclusive rates did not differ between benign and malignant nodules (p = 0.796). Higher inconclusive rates were seen for FNA among cancers regardless of US features, and in the subgroup of size ≥ 40 mm (62.5% vs. 22.9%, p = 0.028). Eleven cancers were diagnosed with CNB (36.7%, 11/30), while none was diagnosed using FNA. CONCLUSION In this experimental study using surgical specimens, CNB showed a potential to provide improved diagnostic sensitivity for thyroid cancer, especially when a conclusive diagnosis is limited with FNA.
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14
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Park JY, Yi SY, Baek SH, Lee YH, Kwon HJ, Park HJ. Diagnostic efficacy, performance and safety of side-cut core needle biopsy for thyroid nodules: comparison of automated and semi-automated biopsy needles. Endocrine 2022; 76:341-348. [PMID: 35032314 DOI: 10.1007/s12020-022-02980-6] [Citation(s) in RCA: 5] [Impact Index Per Article: 1.7] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 09/25/2021] [Accepted: 01/09/2022] [Indexed: 01/20/2023]
Abstract
PURPOSE This study was performed to compare the utility of the semi-automated and automated side-cut core biopsy needles for thyroid nodules. METHODS Between January 2014 and March 2020, biopsy was performed for 278 thyroid nodules using the semi-automated core needle and for 225 nodules using the automated core needle. Nondiagnostic rate, inconclusive rate, diagnostic performance and complication rates were evaluated and compared between two core needle types. RESULTS There were 1.2% (6/503) nondiagnostic results and 15.9% (80/503) inconclusive results. Nondiagnostic rate between two needle types was not significantly different. The semi-automated type (33/278, 11.9%) showed lower inconclusive rate than the automated type (47/225, 20.9%) (p = 0.006). The sensitivity, specificity, PPV, NPV and diagnostic accuracy for diagnosis of malignancy of the semi-automated type were 70.18, 100, 100, 84.96 and 88.89%, respectively; the corresponding rates of automated type were 70.45, 100, 100, 86.6, and 89.84%. There were 12 minor complications: four hematomas (4/278, 1.4%) for the semi-automated type and eight hematomas (8/225, 3.6%) for the automated type, which difference was not statistically significant. CONCLUSION Core needle biopsy for thyroid nodules using either the semi-automated or automated needle is a safe diagnostic tool. Semi-automated needle has lower inconclusive rate than automated needle.
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Affiliation(s)
- Ji Yeon Park
- Department of Radiology, Inje University Ilsan Paik Hospital, Goyang, Republic of Korea
| | - Seong Yoon Yi
- Division of Hematology-Oncology, Department of Internal Medicine, Inje University Ilsan Paik Hospital, Goyang, Republic of Korea.
| | - Soo Heui Baek
- Department of Radiology, Daerim St. Mary's Hospital, Seoul, Republic of Korea
| | - Yu Hyun Lee
- Department of Radiology, Myongji Hospital, Hanyang University College of Medicine, Goyang, Republic of Korea
| | - Heon-Ju Kwon
- Department of Radiology, Kangbuk Samsung Hospital, Sungkyunkwan University School of Medicine, Seoul, Republic of Korea
| | - Hee Jin Park
- Department of Radiology, Kangbuk Samsung Hospital, Sungkyunkwan University School of Medicine, Seoul, Republic of Korea
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15
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Hong MJ, Ahn HS, Ha SM, Park HJ, Oh J. Quantitative analysis of vascularity for thyroid nodules on ultrasound using superb microvascular imaging: Can nodular vascularity differentiate between malignant and benign thyroid nodules? Medicine (Baltimore) 2022; 101:e28725. [PMID: 35119020 PMCID: PMC8812680 DOI: 10.1097/md.0000000000028725] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.3] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 11/26/2020] [Revised: 12/23/2021] [Accepted: 01/11/2022] [Indexed: 01/04/2023] Open
Abstract
This study aimed to investigate the utility of adding superb microvascular imaging (SMI) to B-mode ultrasound (US) for distinguishing between benign and malignant thyroid nodules and evaluate the usefulness of SMI quantification of nodular vascularity for diagnosing thyroid cancer.The malignancy likelihood was scored for 3 datasets before versus after additional color Doppler imaging or SMI using 4-scale visual analysis (i.e., B-mode US alone, B-mode US + color Doppler image, and B-mode US + SMI). Further, the SMI pixel count was measured in the region of interest, including the whole nodule, on the longitudinal view. It was compared between benign and malignant nodules and analyzed according to the US patterns of thyroid nodules based on the Korean thyroid imaging reporting and data system. We calculated the area under the receiver operating characteristic curve values, sensitivities, and specificities.There was no significant difference in the area under the receiver operating characteristic curve values among B-mode, B-mode + color Doppler, and B-mode + SMI. However, the SMI pixel count was significantly higher in malignant thyroid nodules than in benign ones. The optimal cut-off value for the SMI pixel count for predicting malignant thyroid nodules obtained using a receiver operating characteristic curve was 17 (40.54% in sensitivity, 91.3% in specificity). Analysis based on the US pattern of thyroid nodules revealed significant differences in the nodules with low-to-intermediate suspicious US features between malignant and benign nodules.Quantification analysis of vascularity using SMI can differentiate malignant thyroid nodules from benign ones.
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Affiliation(s)
- Min Ji Hong
- Department of Radiology, Chung-Ang University Hospital, Chung-Ang University College of Medicine, Seoul, Republic of Korea
| | - Hye Shin Ahn
- Department of Radiology, Chung-Ang University Hospital, Chung-Ang University College of Medicine, Seoul, Republic of Korea
| | - Su Min Ha
- Department of Radiology, Seoul National University Hospital, Seoul University College of Medicine, Seoul, Republic of Korea
| | - Hyun Jeong Park
- Department of Radiology, Chung-Ang University Hospital, Chung-Ang University College of Medicine, Seoul, Republic of Korea
| | - Jiyun Oh
- Department of Radiology, Chung-Ang University Hospital, Chung-Ang University College of Medicine, Seoul, Republic of Korea
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16
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Kim JY, Chang S, Kwon AY, Park EY, Kim TH, Choi S, Lee M, Oh YL. Core needle biopsy and ultrasonography are superior to fine needle aspiration in the management of follicular variant papillary thyroid carcinomas. Endocrine 2022; 75:437-446. [PMID: 34505274 DOI: 10.1007/s12020-021-02864-1] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 05/18/2021] [Accepted: 08/31/2021] [Indexed: 11/29/2022]
Abstract
PURPOSE Follicular variant papillary thyroid carcinoma (FVPTC) is a problematic entity. FVPTCs are often misdiagnosed by the standard fine needle aspiration (FNA); in addition, FVPTCs represent a mixed group of tumors with two biologically distinct subtypes: The indolent encapsulated FVPTC and the aggressive infiltrative FVPTC. Recent changes in guidelines suggests that FVPTC management may be improved if subtypes can be determined preoperatively. Preoperative assays, FNA, core needle biopsy (CNB), and ultrasonography (US) were compared for their ability to identify and subtype FVPTCs to determine the most appropriate test to manage FVPTCs. METHODS The preoperative assays and clinicopathologic variables of 255 resected FVPTCs cases at Samsung Medical Center between 2012 and 2016 were retrospectively evaluated. RESULTS CNB had the overall best ability to manage FVPTCs with the highest rate of diagnosis indicating surgery, lowest rate of inconclusive results, high sensitivity (88.9%), specificity (87.7%), negative predictive value (97.0%), diagnostic odds ratio (DOR; 56.9), and excellent predictive ability (AUC 0.906) for differentiating FVPTC subtypes. US had a moderate DOR (12.8), good predictive ability (AUC 0.802), high sensitivity (75.0%) and specificity (81.0%). CNB and US both had significantly higher accuracy for discriminating FVPTC subtypes than FNA (AUC 0.908 and 0.877 > 0.671; p < 0.05). The excellent performance of CNB could be attributed to distinct histologic differences between FVPTC subtypes. CONCLUSION CNB and US had superior performance to FNA in the identification and subtyping of FVPTC. In institutions with skilled and experienced operators, CNB is the preferred method for evaluating possible FVPTC lesions.
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Affiliation(s)
- Ji-Ye Kim
- Department of Pathology, Ilsan Paik Hospital, Inje University College of Medicine, Goyang, Republic of Korea
| | - Sunhee Chang
- Department of Pathology, Ilsan Paik Hospital, Inje University College of Medicine, Goyang, Republic of Korea
| | - Ah-Young Kwon
- Department of Pathology, CHA Bundang Medical Center, CHA University, Seongnam, Republic of Korea
| | - Eun Young Park
- Biostatistics Collaboration Team, Research Core Center, National Cancer Center, Goyang, Republic of Korea
| | - Tae Hyuk Kim
- Division of Endocrinology & Metabolism, Department of Medicine, Thyroid Center, Samsung Medical Center, Sungkyunkwan University School of Medicine, Seoul, Republic of Korea
| | - Sangjoon Choi
- Department of Pathology and Translational Genomics, Samsung Medical Center, Sungkyunkwan University School of Medicine, Seoul, Republic of Korea
| | - Minju Lee
- Department of Pathology and Translational Genomics, Samsung Medical Center, Sungkyunkwan University School of Medicine, Seoul, Republic of Korea
- Forensic Medicine Investigation Division, Seoul Institute National Forensic Service, Seoul, Republic of Korea
| | - Young Lyun Oh
- Department of Pathology and Translational Genomics, Samsung Medical Center, Sungkyunkwan University School of Medicine, Seoul, Republic of Korea.
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17
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Kim K, Bae JS, Kim JS, Jung SL, Jung CK. Diagnostic Performance of Thyroid Core Needle Biopsy Using the Revised Reporting System: Comparison with Fine Needle Aspiration Cytology. Endocrinol Metab (Seoul) 2022; 37:159-169. [PMID: 35255608 PMCID: PMC8901962 DOI: 10.3803/enm.2021.1299] [Citation(s) in RCA: 6] [Impact Index Per Article: 2.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 10/11/2021] [Accepted: 01/06/2022] [Indexed: 11/11/2022] Open
Abstract
BACKGROUND We aim to validate the diagnostic performance of thyroid core needle biopsy (CNB) for diagnosing malignancy in clinical settings to align with the changes made in recently updated thyroid CNB guidelines. METHODS We retrospectively analyzed 1,381 thyroid CNB and 2,223 fine needle aspiration (FNA) samples. The FNA and CNB slides were interpreted according to the Bethesda System for Reporting Thyroid Cytopathology and updated practice guidelines for thyroid CNB, respectively. RESULTS Compared to FNA, CNB showed lower rates of inconclusive results categories I (2.8% vs. 11.2%) and III (1.2% vs. 6.2%), and higher rates of categories II (60.9% vs. 50.4%) and IV (17.5% vs. 2.0%). The upper and lower bounds of the risk of malignancy (ROM) for category IV of CNB were 43.2% and 26.6%, respectively. The CNB subcategory IVb with nuclear atypia had a higher ROM than the subcategory without nuclear atypia (40%-62% vs. 23%-36%). In histologically confirmed cases, there was no significant difference in the diagnostic performance between CNB and FNA for malignancy. However, neoplastic diseases were more frequently detected by CNB than by FNA (88.8% vs. 77.6%, P=0.046). In category IV, there was no difference in unnecessary surgery rate between CNB and FNA (4.7% vs. 6.9%, P=0.6361). CONCLUSION Thyroid CNB decreased the rate of inconclusive results and showed a higher category IV diagnostic rate than FNA. The revised guidelines for thyroid CNB proved to be an excellent reporting system for assessing thyroid nodules.
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Affiliation(s)
- Kwangsoon Kim
- Department of Surgery, College of Medicine, The Catholic University of Korea, Seoul,
Korea
| | - Ja Seong Bae
- Department of Surgery, College of Medicine, The Catholic University of Korea, Seoul,
Korea
| | - Jeong Soo Kim
- Department of Surgery, College of Medicine, The Catholic University of Korea, Seoul,
Korea
| | - So Lyung Jung
- Department of Radiology, College of Medicine, The Catholic University of Korea, Seoul,
Korea
| | - Chan Kwon Jung
- Department of Hospital Pathology, College of Medicine, The Catholic University of Korea, Seoul,
Korea
- Cancer Research Institute, College of Medicine, The Catholic University of Korea, Seoul,
Korea
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18
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Kim J, Shin JH, Oh YL, Hahn SY, Park KW. Approach to Bethesda system category III thyroid nodules according to US-risk stratification. Endocr J 2022; 69:67-74. [PMID: 34408101 DOI: 10.1507/endocrj.ej21-0300] [Citation(s) in RCA: 4] [Impact Index Per Article: 1.3] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Indexed: 11/23/2022] Open
Abstract
This study evaluated how to manage Bethesda category III (Bethesda III) (atypia of undetermined significance/follicular lesion of undetermined significance [AUS/FLUS]) thyroid nodules according to the Korean Thyroid Imaging Reporting and Data System (K-TIRADS) to reduce unnecessary surgeries. A total of 161 thyroid nodules diagnosed as Bethesda III underwent surgery from 2016 to 2019. Ultrasonography-guided fine-needle aspiration (US-FNA) or core needle biopsy (CNB) was used for repeat examination. K-TIRADS category was assigned to the thyroid nodules. The proportion of malignancy in Bethesda III nodules confirmed by surgery were significantly increased in proportion relative to K-TIRADS with 60.0% low suspicion, 88.2% intermediate suspicion, and 100% high suspicion nodules (p < 0.001). The proportion of malignancy in AUS and FLUS were significantly different (94.2% vs. 40.0% p = 0.003). The proportion of malignancy in AUS increased with K-TIRADS categories, but there was no difference in FLUS. All K-TIRADS high suspicion nodules were AUS as papillary carcinomas (99%), while 80% of FLUS nodules and 50% of follicular carcinomas showed K-TIRADS low suspicion. In 116 nodules with repeat FNA or CNB after initial Bethesda III results, the conclusive result rate was significantly increased in proportion to K-TIRADS with 58.3% low suspicion, 83.3% intermediate suspicion, and 88.8% high suspicion nodules (p = 0.015). K-TIRADS low suspicion nodules of Bethesda III nodules should be managed after risk-benefit consideration rather than immediate surgery or repeat examination. K-TIRADS for Bethesda III nodules can predict papillary carcinoma well, but not follicular carcinoma.
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Affiliation(s)
- Jieun Kim
- Department of Radiology, Samsung Medical Center, Sungkyunkwan University School of Medicine, Seoul, Republic of Korea
- Department of Radiology, Inje University Haeundae Paik Hospital, Busan, Republic of Korea
| | - Jung Hee Shin
- Department of Radiology, Samsung Medical Center, Sungkyunkwan University School of Medicine, Seoul, Republic of Korea
| | - Young Lyun Oh
- Department of Pathology, Samsung Medical Center, Sungkyunkwan University School of Medicine, Seoul, Republic of Korea
| | - Soo Yeon Hahn
- Department of Radiology, Samsung Medical Center, Sungkyunkwan University School of Medicine, Seoul, Republic of Korea
| | - Ko Woon Park
- Department of Radiology, Samsung Medical Center, Sungkyunkwan University School of Medicine, Seoul, Republic of Korea
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Yoo MH, Kim HJ, Choi IH, Park S, Yun S, Park HK, Byun DW, Suh K. Efficacy of Differential Diagnosis of Thyroid Nodules by Shear Wave Elastography-the Stiffness Map. J Endocr Soc 2021; 5:bvab154. [PMID: 34703960 PMCID: PMC8533983 DOI: 10.1210/jendso/bvab154] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 04/12/2021] [Indexed: 01/04/2023] Open
Abstract
BACKGROUND Fine needle aspiration is the gold standard for differential diagnosis of thyroid nodules; however, the malignancy rate for indeterminate cytology is 20% to 50%. OBJECTIVE We evaluated the efficacy of shear wave elastography added to ultrasonography for differential diagnosis of thyroid nodules. METHODS We retrospectively reviewed the medical records of 258 consecutive patients. Thyroid nodules were divided into 4 categories according to maximum elasticity (EMax) and nodule depth/width (D/W) ratio: Category 1 (EMax ≥ 42.6 kPa; D/W < 0.9); Category 2 (EMax < 42.6 kPa; D/W < 0.9); Category 3 (EMax ≥ 42.6 kPa; D/W ≥ 0.9); and Category 4 (EMax < 42.6 kPa; D/W ≥ 0.9). The EMax cutoff value was set using receiver operating characteristic (ROC) curve analysis to predict nodular hyperplasia (NH) vs follicular neoplasm (FN). Cutoff value for nodule D/W ratio was set using ROC curve analysis for malignancy. RESULTS NH was the most prevalent pathology group in Category 1, FN in Category 2, and papillary thyroid carcinoma in Category 3. Category 3 demonstrated the highest rate of malignancy (81.8%) and had 55.4% sensitivity and 90% specificity for predicting malignancy. When assessing the benign pathology of NH in follicular patterned lesion, Category 1 demonstrated the highest NH prevalence of 88.9% (34/37) and had 73.9% sensitivity and 85.0% specificity. CONCLUSION The performance for malignancy was highest in Category 3 and predictive ability for benign pathology of NH in follicular lesion was highest in Category 1. The information of EMax and nodule D/W ratio was useful to predict the pathology of thyroid nodules.
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Affiliation(s)
- Myung Hi Yoo
- Division of Endocrinology and Metabolism, Department of Internal Medicine, Soonchunhyang University Hospital, Soonchunhyang University College of Medicine, Seoul 04401, Korea
- Elim Thyroid Clinic, Seoul 06520, Korea
| | - Hye Jeong Kim
- Division of Endocrinology and Metabolism, Department of Internal Medicine, Soonchunhyang University Hospital, Soonchunhyang University College of Medicine, Seoul 04401, Korea
| | - In Ho Choi
- Department of Pathology, Soonchunhyang University Hospital, Seoul 04401, Korea
| | - Suyeon Park
- Department of Biostatics and Data Innovation, Soonchunhyang University, College of Medicine, Seoul 04401, Korea
- Department of Applied Statistics, Chung-Ang University, Seoul 06974, Korea
| | - Sumi Yun
- Department of Diagnostic Pathology, Samkwang Medical Laboratories, Seoul 06742, Korea
| | - Hyeong Kyu Park
- Division of Endocrinology and Metabolism, Department of Internal Medicine, Soonchunhyang University Hospital, Soonchunhyang University College of Medicine, Seoul 04401, Korea
| | - Dong Won Byun
- Division of Endocrinology and Metabolism, Department of Internal Medicine, Soonchunhyang University Hospital, Soonchunhyang University College of Medicine, Seoul 04401, Korea
| | - Kyoil Suh
- Division of Endocrinology and Metabolism, Department of Internal Medicine, Soonchunhyang University Hospital, Soonchunhyang University College of Medicine, Seoul 04401, Korea
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An HJ, Kim MH, Na JM, Yang JW, Baek HJ, Ryu KH, Song DH. Diagnostic Utility of p62 Expression in Intranuclear Inclusions in Thyroid Core Needle Biopsy Specimens. In Vivo 2021; 35:1769-1775. [PMID: 33910861 DOI: 10.21873/invivo.12436] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/13/2021] [Revised: 02/03/2021] [Accepted: 02/10/2021] [Indexed: 11/10/2022]
Abstract
BACKGROUND/AIM Core needle biopsy (CNB) has been widely used as an alternative method to ultrasound-guided fine-needle aspiration cytology for histological diagnosis of thyroid specimens. However, nuclear artifactual vacuoles (NuVas) produced during tissue processing can be very difficult and sometimes impossible to distinguish from intranuclear inclusions (NuIns). P62 is an autophagy receptor that recognizes, targets, and eliminates toxic cellular materials during autophagy. Herein, we examined the utility of p62 immunohistochemical staining to detect NuIns in thyroid core needle biopsy specimens. PATIENTS AND METHODS Thirty-five thyroid CNB slides from 32 patients and corresponding resection specimens stained with hematoxylin and eosin were reviewed by two pathologists. The immunohistochemical staining pattern of p62 was used to differentiate NuIns from NuVas. The diameter of each nucleus (A) and NuIn (B) was measured, and the number of p62-expressing NuIn-positive (p62In) cells was counted using 1/2 (B/A) and 1/3 (B/A) criteria. The criterion of 1/3 includes NuIns larger than 1/3 and smaller than 1/2 of the nuclear diameter. The criteria of 1/2 includes NuIns larger than 1/2 of the nuclear diameter. RESULTS By applying the 1/2 criterion, there were no p62In cells in follicular adenoma (FA) samples. However, in papillary thyroid carcinoma (PTC) samples, 22 of 25 specimens exhibited p62In cells. The sensitivity and specificity to distinguish FA from PTC using the 1/2 criterion were 0.88 and 1.00, respectively. By applying the 1/3 criterion, there was one p62In cell hit in FA samples. However, 23 of 25 PTC specimens showed p62In cells. The sensitivity and specificity to distinguish FA from PTC using the 1/3 criterion were 1.00 and 0.90, respectively. CONCLUSION P62 is a useful marker for distinguishing FA and PTC based on CNB specimens. We suggest the 1/2 criteria for identifying p62In cells.
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Affiliation(s)
- Hyo Jung An
- Department of Pathology, Gyeongsang National University Changwon Hospital, Changwon, Republic of Korea.,Department of Pathology, Gyeongsang National University School of Medicine, Jinju, Republic of Korea.,Department of Pathology, Gyeongsang Institute of Health Science, Jinju, Republic of Korea
| | - Min Hye Kim
- Department of Pathology, Gyeongsang National University Hospital, Jinju, Republic of Korea
| | - Ji Min Na
- Department of Pathology, Gyeongsang National University Hospital, Jinju, Republic of Korea
| | - Jung Wook Yang
- Department of Pathology, Gyeongsang National University School of Medicine, Jinju, Republic of Korea.,Department of Pathology, Gyeongsang Institute of Health Science, Jinju, Republic of Korea.,Department of Pathology, Gyeongsang National University Hospital, Jinju, Republic of Korea
| | - Hye Jin Baek
- Department of Radiology, Gyeongsang National University Changwon Hospital, Changwon, Republic of Korea.,Department of Radiology, Gyeongsang National University School of Medicine, Jinju, Republic of Korea.,Department of Radiology, Institute of Health Sciences, Gyeongsang National University School of Medicine, Jinju, Republic of Korea
| | - Kyeong Hwa Ryu
- Department of Radiology, Gyeongsang National University Changwon Hospital, Changwon, Republic of Korea.,Department of Radiology, Gyeongsang National University School of Medicine, Jinju, Republic of Korea.,Department of Radiology, Institute of Health Sciences, Gyeongsang National University School of Medicine, Jinju, Republic of Korea
| | - Dae Hyun Song
- Department of Pathology, Gyeongsang National University Changwon Hospital, Changwon, Republic of Korea; .,Department of Pathology, Gyeongsang National University School of Medicine, Jinju, Republic of Korea.,Department of Pathology, Gyeongsang Institute of Health Science, Jinju, Republic of Korea
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21
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Hahn SY, Shin JH, Oh YL, Park KW. Ultrasonographic characteristics of medullary thyroid carcinoma according to nodule size: application of the Korean Thyroid Imaging Reporting and Data System and American Thyroid Association guidelines. Acta Radiol 2021; 62:474-482. [PMID: 32493032 DOI: 10.1177/0284185120929699] [Citation(s) in RCA: 5] [Impact Index Per Article: 1.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 12/14/2022]
Abstract
BACKGROUND Few studies have categorized ultrasound (US) findings of various sized medullary thyroid carcinomas (MTCs) according to updated guidelines. PURPOSE To evaluate and compare the differences in US findings of MTC according to nodule size, using the Korean Thyroid Imaging Reporting and Data System (K-TIRADS) and American Thyroid Association (ATA) guidelines. MATERIAL AND METHODS The study included 119 patients with 129 MTC nodules, which were surgically confirmed at our institution between March 1999 and September 2017. Nodules were divided into large (≥1.0 cm) and small (<1.0 cm) groups. US images were analyzed according to the K-TIRADS and ATA guidelines. The differences in US characteristics between small and large nodules were compared using Fisher's exact or Chi-square tests. RESULTS Of 129 MTC nodules, 84 (65.1%) were large nodules and 45 (34.9%) were small nodules. According to the nodule size, small MTC nodules were classified more commonly as high suspicion by K-TIRADS and ATA (95.6% and 93.3%, respectively) (P < 0.001), but presented neither cystic change, isoechogenicity, nor low suspicion category by K-TIRADS and ATA. In contrast, large MTC nodules showed more frequently cystic change (15.5%), isoechogenicity (16.7%), smooth margins (50%), or low or intermediate suspicion US features by K-TIRADS and ATA (59.6% and 36.0%, respectively) (all P values < 0.001). CONCLUSION Most small MTC nodules are classified as high suspicion on US, whereas large MTC nodules are diagnosed more frequently as low or intermediate suspicion by K-TIRADS and ATA.
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Affiliation(s)
- Soo Yeon Hahn
- Department of Radiology and Center for Imaging Science, Thyroid Center, Samsung Medical Center, Sungkyunkwan University School of Medicine, Seoul, Republic of Korea
| | - Jung Hee Shin
- Department of Radiology and Center for Imaging Science, Thyroid Center, Samsung Medical Center, Sungkyunkwan University School of Medicine, Seoul, Republic of Korea
| | - Young Lyun Oh
- Department of Pathology, Thyroid Center, Samsung Medical Center, Sungkyunkwan University School of Medicine, Seoul, Republic of Korea
| | - Ko Woon Park
- Department of Radiology and Center for Imaging Science, Thyroid Center, Samsung Medical Center, Sungkyunkwan University School of Medicine, Seoul, Republic of Korea
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Cho YY, Chung YJ, Kim HS. Malignancy Rate of Bethesda Class III Thyroid Nodules Based on the Presence of Chronic Lymphocytic Thyroiditis in Surgical Patients. Front Endocrinol (Lausanne) 2021; 12:745395. [PMID: 34659127 PMCID: PMC8515134 DOI: 10.3389/fendo.2021.745395] [Citation(s) in RCA: 2] [Impact Index Per Article: 0.5] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 07/22/2021] [Accepted: 09/13/2021] [Indexed: 01/21/2023] Open
Abstract
BACKGROUND Hashimoto's thyroiditis (HT), also known as chronic lymphocytic thyroiditis (CLT), may interfere with the accurate cytological diagnosis of thyroid nodules. Recently, HT has been considered a premalignant condition for thyroid cancer development. The diagnosis of atypia of undetermined significance/follicular lesions of undetermined significance (AUS/FLUS) thyroid nodules is challenging and evidence for the malignancy risk of AUS/FLUS thyroid nodules coexisting with CLT is scarce. Therefore, we assessed the malignancy risk of AUS/FLUS thyroid nodules according to the presence of background CLT. METHODS This study included 357 surgically resected thyroid nodules with AUS/FLUS cytology. Cases with concomitant malignant nodules were excluded. CLT was defined based on the pathologic report after thyroid surgery. RESULTS Among 357 tumors, 130 tumors (36%) were confirmed to have coexisting CLT, and 170 tumors (48%) were determined to be malignant after thyroidectomy. Malignancy rates were similar in both groups (48% in each) regardless of background CLT (62/130 with CLT vs. 108/227 without CLT). In the group with CLT, thyroiditis was more frequent in the final pathology (12% with CLT vs. 1% without CLT, P = 0.003). In multivariate analysis, positive BRAFV600E mutation, highly suspicious sonographic features (K-TIRADS 5), and smaller thyroid nodules were significant factors for thyroid malignancies. CONCLUSION The malignancy rate of thyroid nodules with AUS/FLUS cytology was comparable irrespective of the presence of underlying CLT.
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Affiliation(s)
- Yoon Young Cho
- Division of Endocrinology and Metabolism, Department of Medicine, Soonchunhyang University Bucheon Hospital, College of Medicine, Soonchunhyang University, Bucheon, South Korea
| | - Yun Jae Chung
- Division of Endocrinology and Metabolism, Department of Internal Medicine, College of Medicine, Chung-Ang University, Seoul, South Korea
- *Correspondence: Yun Jae Chung,
| | - Hee Sung Kim
- Department of Pathology, College of Medicine, Chung-Ang University, Seoul, South Korea
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Liu J, Guo Y, Xiao J, Chen L, Liang Z. Comparison of the Efficacy and Safety of the American Thyroid Association Guidelines and American College of Radiology TI-RADS. Endocr Pract 2020; 27:661-667. [PMID: 34250908 DOI: 10.1016/j.eprac.2020.11.013] [Citation(s) in RCA: 3] [Impact Index Per Article: 0.6] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 09/06/2020] [Revised: 10/16/2020] [Accepted: 11/10/2020] [Indexed: 01/25/2023]
Abstract
OBJECTIVE To evaluate the 2015 American Thyroid Association (ATA) guidelines and 2017 American College of Radiology (ACR) Thyroid Imaging, Reporting and Data System (TI-RADS) for their efficacy in predicting malignant thyroid nodules and safety in recommending fine needle aspiration (FNA). METHODS We reviewed data of 970 thyroid nodules from 908 patients with core needle biopsy pathology. We calculated the accuracy, sensitivity, specificity, positive predictive value, and negative predictive value for each guideline to predict malignancies. We compared the areas under the curve and FNA recommendations between the 2 guidelines. RESULTS According to the core needle biopsy pathology, 59.9% (581/970) of the thyroid nodules were malignant. Accuracy, sensitivity, specificity, positive predictive value, and negative predictive value was 68%, 91%, 33%, 67%, and 70%, respectively, for the ATA guidelines and 70%, 84%, 49%, 71%, and 68%, respectively, for the ACR TI-RADS. Areas under the curve (ATA: 0.71 vs ACR TI-RADS: 0.74; P = .054) were similar when predicting malignancies. For the 545 nodules with maximum diameter ≥1.0 cm, the ACR TI-RADS recommended FNA less often than the ATA guidelines (83.3% [454/545] vs 87.7% [478/545]; P = .01). For the 321 malignant nodules with maximum diameter ≥1.0 cm, the proportions of FNA recommendations were not significantly different (ACR TI-RADS: 90.7% [291/321] vs ATA: 92.5% [297/321]; P = .06). CONCLUSION The 2015 ATA guidelines and 2017 ACR TI-RADS showed a similar ability in predicting malignancies. Reducing FNA recommendations by the ACR TI-RADS would not lead to a significant decrease in the FNA recommendations given for malignancies with maximum diameter ≥1.0 cm.
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Affiliation(s)
- Jinghua Liu
- Department of Ultrasound, Peking University First Hospital, 8 Xishiku Street, Xicheng District, Beijing, China
| | - Yajun Guo
- Department of Epidemiology, Tulane University School of Public Health and Tropical Medicine, 1440 Canal Street, New Orleans, Louisiana, USA
| | - Jiangxi Xiao
- Department of Radiology, Peking University First Hospital, 8 Xishiku Street, Xicheng District, Beijing, China.
| | - Luzeng Chen
- Department of Ultrasound, Peking University First Hospital, 8 Xishiku Street, Xicheng District, Beijing, China.
| | - Zhenwei Liang
- Department of Ultrasound, Peking University First Hospital, 8 Xishiku Street, Xicheng District, Beijing, China
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Yoon JH, Lee HS, Kim EK, Moon HJ, Park VY, Kwak JY. Cytopathologic criteria and size should be considered in comparison of fine-needle aspiration vs. core-needle biopsy for thyroid nodules: results based on large surgical series. Endocrine 2020; 70:558-565. [PMID: 32656693 DOI: 10.1007/s12020-020-02416-z] [Citation(s) in RCA: 7] [Impact Index Per Article: 1.4] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 04/22/2020] [Accepted: 07/04/2020] [Indexed: 01/21/2023]
Abstract
PURPOSE To evaluate and compared the diagnostic performances of FNA and CNB using various cytopathologic criteria and size subgroups to see how the comparison results differ accordingly. METHODS From May 2012 to May 2019, 8187 thyroid nodules in 8139 patients who had undergone preoperative US-guided FNA or CNB at outside clinics were included in this retrospective study (mean size: 11.9 ± 9.5 mm). Preoperative US-FNA was performed in 7496 (91.6%) nodules and US-CNB was performed in 691 (8.4%) nodules. Propensity score matching was used to compare the sensitivities between FNA and CNB in diagnosis of malignancy and neoplasm according to different cytologic test criteria. RESULTS Of the 8187 thyroid nodules, 7833 (95.7%) were malignant and 354 (4.3%) were benign. Mean size of the thyroid nodules in the CNB group was significantly larger than the FNA group, 15.7 ± 12.7 mm vs. 11.6 ± 9.0 mm, respectively (P < 0.001). After matching, sensitivity in the CNB group were significantly higher in the total population, and in subgroups <10 mm for criteria 1 and 2 (all P < 0.05, respectively). No significant differences were seen between the sensitivities of FNA and CNB for nodules ≥10 mm regardless of criteria in diagnosis of malignancy or neoplasm (all P > 0.05, respectively). CONCLUSIONS Results comparing sensitivities between FNA and CNB differ according to the different cytopathologic criteria used for calculation. CNB has significantly higher sensitivity to FNA in subcentimeter nodules when using criteria 1 or 2. Diagnostic sensitivities did not show significant differences for nodules ≥10 mm regardless of the cytopathologic criteria used, that should be considered in selecting biopsy methods.
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Affiliation(s)
- Jung Hyun Yoon
- Department of Radiology, Severance Hospital, Research Institute of Radiological Science, Yonsei University, College of Medicine, Seoul, Republic of Korea
| | - Hye Sun Lee
- Biostatistics Collaboration Unit, Yonsei University, College of Medicine, Seoul, Republic of Korea
| | - Eun-Kyung Kim
- Department of Radiology, Yongin Severance Hospital, Yonsei University, College of Medicine, Yongin, Republic of Korea
| | - Hee Jung Moon
- Department of Radiology, Severance Hospital, Research Institute of Radiological Science, Yonsei University, College of Medicine, Seoul, Republic of Korea
| | - Vivian Youngjean Park
- Department of Radiology, Severance Hospital, Research Institute of Radiological Science, Yonsei University, College of Medicine, Seoul, Republic of Korea
| | - Jin Young Kwak
- Department of Radiology, Severance Hospital, Research Institute of Radiological Science, Yonsei University, College of Medicine, Seoul, Republic of Korea.
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25
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Na HY, Moon JH, Choi JY, Yu HW, Jeong WJ, Kim YK, Choe JY, Park SY. Preoperative diagnostic categories of fine needle aspiration cytology for histologically proven thyroid follicular adenoma and carcinoma, and Hurthle cell adenoma and carcinoma: Analysis of cause of under- or misdiagnoses. PLoS One 2020; 15:e0241597. [PMID: 33147258 PMCID: PMC7641403 DOI: 10.1371/journal.pone.0241597] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/04/2020] [Accepted: 10/17/2020] [Indexed: 11/18/2022] Open
Abstract
Cytologic diagnosis of thyroid follicular adenoma and carcinoma, and Hurthle cell adenoma and carcinoma (FACHAC) is challenging due to cytomorphologic features that overlap with other follicular-patterned lesions. This study was designed to analyze diagnostic categories (DCs) of preoperative fine needle aspiration cytology (FNAC) of histologically proven thyroid FACHACs to evaluate under- or misdiagnoses in FNAC and elucidate potential causes for such phenomena. A total of 104 thyroid nodules with preoperative FNAC which were diagnosed as FACHAC in resection specimens were included in this study. Of these, 66 cases had also undergone thyroid core needle biopsy (CNB); FNAC and CNB DCs were compared in these cases. Various cytologic and histologic parameters were compared between the nodules with different FNAC DCs. After a review of FNAC slides, DCs were re-assigned in 20 (19.2%) out of the 104 cases. Of the 66 cases with CNB diagnoses which were mostly classified as lower DCs in FNAC, 31 (47.0%) were diagnosed as suspicious for a follicular neoplasm in CNB. Cases which were underdiagnosed in FNACs were associated with lower cellularity, predominant macrofollicular pattern, absence of microfollicles arranged in trabecular pattern, and absence of transgressing vessels in cytology smears. High cellularity, microfollicles arranged in trabecular pattern, nucleolar prominence, and large cell dysplasia were more frequently found in malignancy than in benign neoplasm. In conclusion, thyroid FACHACs seem to be under- and misdiagnosed in preoperative FNAC. Innate characteristics of the nodules were associated with under-diagnosis as well as the quality of the FNAC specimens. Certain cytomorphologic features can be helpful in differentiating malignancy among FACHACs.
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Affiliation(s)
- Hee Young Na
- Department of Pathology, Seoul National University Bundang Hospital, Seoul National University College of Medicine, Seoul, Republic of Korea
| | - Jae Hoon Moon
- Department of Internal Medicine, Seoul National University Bundang Hospital, Seoul National University College of Medicine, Seoul, Republic of Korea
| | - June Young Choi
- Department of Surgery, Seoul National University Bundang Hospital, Seoul National University College of Medicine, Seoul, Republic of Korea
| | - Hyeong Won Yu
- Department of Surgery, Seoul National University Bundang Hospital, Seoul National University College of Medicine, Seoul, Republic of Korea
| | - Woo-Jin Jeong
- Department of Otorhinolaryngology–Head and Neck Surgery, Seoul National University Bundang Hospital, Seoul National University College of Medicine, Seoul, Republic of Korea
| | - Yeo Koon Kim
- Department of Radiology, Seoul National University Bundang Hospital, Seoul National University College of Medicine, Seoul, Republic of Korea
| | - Ji-Young Choe
- Department of Pathology, Hallym University Sacred Heart Hospital, Anyang, Republic of Korea
| | - So Yeon Park
- Department of Pathology, Seoul National University Bundang Hospital, Seoul National University College of Medicine, Seoul, Republic of Korea
- * E-mail:
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26
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Gwon HY, Na DG, Noh BJ, Paik W, Yoon SJ, Choi SJ, Shin DR. Thyroid Nodules with Isolated Macrocalcifications: Malignancy Risk of Isolated Macrocalcifications and Postoperative Risk Stratification of Malignant Tumors Manifesting as Isolated Macrocalcifications. Korean J Radiol 2020; 21:605-613. [PMID: 32323506 PMCID: PMC7183826 DOI: 10.3348/kjr.2019.0523] [Citation(s) in RCA: 13] [Impact Index Per Article: 2.6] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/13/2019] [Accepted: 01/19/2020] [Indexed: 12/15/2022] Open
Abstract
Objective To determine the malignancy risk of isolated macrocalcifications (a calcified nodule with complete posterior acoustic shadowing) detected on ultrasonography (US) and to evaluate the postoperative American Thyroid Association (ATA) risk stratification of malignant tumors manifesting as isolated macrocalcifications. Materials and Methods A total of 3852 thyroid nodules (≥ 1 cm) of 3061 consecutive patients who had undergone biopsy between January 2011 and June 2018 were included in this study. We assessed the prevalence, malignancy rate, and size distribution of isolated macrocalcifications and evaluated the histopathologic features and postoperative ATA risk stratification of malignant tumors manifesting as isolated macrocalcifications. Results Isolated macrocalcifications were found in 38 (1.2%) of the 3061 patients. Final diagnosis was established in 30 (78.9%) nodules; seven malignant tumors were diagnosed as papillary thyroid carcinomas (PTCs). The malignancy rate of the isolated macrocalcifications was 23.3% in the 30 nodules with final diagnoses and 18.4% in all nodules. Among the six surgically-treated malignant tumors, five (83.3%) had an extrathyroidal extension (ETE) (minor ETE 1, gross ETE 4), and two (33.3%) had macroscopic lymph node metastasis. Four (66.7%) malignant tumors were categorized as high-risk tumors, one as an intermediate-risk tumor, and one as a low-risk tumor using the ATA risk stratification. Histopathologically, out of the six malignant tumors, ossifications were noted in four (66.7%) and predominant calcifications in two (33.3%). Conclusion The US pattern of isolated macrocalcifications (≥ 1 cm) showed an intermediate malignancy risk (at least 18.4%). All malignant tumors were PTCs, and most showed an aggressive behavior and a high or intermediate postoperative ATA risk.
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Affiliation(s)
- Hye Yun Gwon
- Department of Radiology, GangNeung Asan Hospital, Gangneung, Korea
| | - Dong Gyu Na
- Department of Radiology, GangNeung Asan Hospital, Gangneung, Korea.
| | - Byeong Joo Noh
- Department of Pathology, GangNeung Asan Hospital, Gangneung, Korea
| | - Wooyul Paik
- Department of Radiology, GangNeung Asan Hospital, Gangneung, Korea
| | - So Jin Yoon
- Department of Radiology, GangNeung Asan Hospital, Gangneung, Korea
| | - Soo Jung Choi
- Department of Radiology, GangNeung Asan Hospital, Gangneung, Korea
| | - Dong Rock Shin
- Department of Radiology, GangNeung Asan Hospital, Gangneung, Korea
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27
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Yim Y, Na DG, Ha EJ, Baek JH, Sung JY, Kim JH, Moon WJ. Concordance of Three International Guidelines for Thyroid Nodules Classified by Ultrasonography and Diagnostic Performance of Biopsy Criteria. Korean J Radiol 2020; 21:108-116. [PMID: 31920034 PMCID: PMC6960308 DOI: 10.3348/kjr.2019.0215] [Citation(s) in RCA: 21] [Impact Index Per Article: 4.2] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 03/31/2019] [Accepted: 10/14/2019] [Indexed: 01/29/2023] Open
Abstract
Objective To investigate the concordance of three international guidelines: the Korean Thyroid Association/Korean Society of Thyroid Radiology, American Thyroid Association, and American College of Radiology for thyroid nodules classified by ultrasonography (US) and the diagnostic performance of simulated size criteria for malignant biopsies. Materials and Methods A total of 2586 thyroid nodules (≥ 1 cm) were collected from two multicenter study datasets. The classifications of the thyroid nodules were based on three different guidelines according to US categories for malignancy risk, and the concordance rate between the different guidelines was calculated for the classified nodules. In addition, the diagnostic performance of criteria related to four different simulated biopsy sizes was evaluated. Results The concordance rate of nodules classified as high- or intermediate-suspicion was high (84.1–100%), but low-suspicion or mildly-suspicious nodules exhibited relatively low concordance (63.8–83.8%) between the three guidelines. The differences in sensitivity, specificity, and accuracy between the guidelines were 0.7–19.8%, 0–40.9%, and 0.1–30.5%, respectively, when the original biopsy criteria were applied. The differences decreased to 0–5.9%, 0–10.9%, and 0.1–8.2%, respectively, when simulated, similar biopsy size criteria were applied. The unnecessary biopsy rate calculated with the original criteria (0–33.8%), decreased with the simulated biopsy size criteria (0–8.7%). Conclusion We found a high concordance between the three guidelines for high- or intermediate-suspicion nodules, and the diagnostic performance of the biopsy criteria was approximately equivalent for each simulated size criterion. The difference in diagnostic performance between the three guidelines is mostly influenced by the various size thresholds for biopsies.
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Affiliation(s)
- Younghee Yim
- Department of Radiology, College of Medicine, Kangwon National University, Kangwon National University Hospital, Chuncheon, Korea
| | - Dong Gyu Na
- Department of Radiology, GangNeung Asan Hospital, University of Ulsan College of Medicine, Gangneung, Korea.
| | - Eun Ju Ha
- Department of Radiology, Ajou University, School of Medicine, Suwon, Korea
| | - Jung Hwan Baek
- Department of Radiology and Research Institute of Radiology, University of Ulsan College of Medicine, Asan Medical Center, Seoul, Korea
| | - Jin Yong Sung
- Department of Radiology, Thyroid Center, Daerim St. Mary's Hospital, Seoul, Korea
| | - Ji Hoon Kim
- Department of Radiology, Seoul National University Hospital, Seoul National University College of Medicine, Seoul, Korea
| | - Won Jin Moon
- Department of Radiology, Konkuk University Medical Center, Konkuk University School of Medicine, Seoul, Korea
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28
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Hong MJ, Na DG, Lee H. Diagnostic Efficacy and Safety of Core Needle Biopsy as a First-Line Diagnostic Method for Thyroid Nodules: A Prospective Cohort Study. Thyroid 2020; 30:1141-1149. [PMID: 32228167 DOI: 10.1089/thy.2019.0444] [Citation(s) in RCA: 13] [Impact Index Per Article: 2.6] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Indexed: 11/13/2022]
Abstract
Background: The diagnostic role of ultrasonography (US)-guided core needle biopsy (CNB) as a first-line diagnostic method for thyroid nodules remains controversial. This study was performed to determine the diagnostic efficacy and safety of CNB as a first-line diagnostic method for thyroid nodules. Methods: From February 2016 to January 2018, CNB was prospectively performed by an experienced radiologist in all consecutive patients with thyroid nodules indicated for fine-needle aspiration (FNA). Three patients refused this protocol. Finally, 212 consecutive patients with 248 thyroid nodules were enrolled in this prospective study. Combined CNB/FNA was selectively performed in 43 patients. The diagnostic efficacy of CNB was evaluated by the rate of inconclusive results (nondiagnostic or indeterminate results), and its feasibility was estimated by calculating the successful biopsy rate and by measuring the procedure time from the time of the initial skin puncture to the last withdrawal of the biopsy needle from the skin. The safety of the procedure was evaluated by the major and minor complication rates. A US evaluation was performed before and after manual self-compression to assess for hemorrhage at the biopsy site, and delayed complications were assessed 5-7 days after the biopsy. Any hemorrhage that did not require hospitalization was classified as a minor complication. Results: CNB was performed once (n = 125, 50.4%), twice (n = 122, 49.2%), or three times (n = 1, 0.4%) per nodule. The diagnostic results of CNB were as follows: nondiagnostic (0.8%), benign (63.3%), indeterminate (10.1%), follicular neoplasm (3.2%), suspected malignancy (2.4%), and malignancy (20.1%); the rate of inconclusive results was 10.9%. The successful biopsy rate of CNB was 100%, and the median procedure time was 102 seconds (interquartile range 51-181 seconds). There were no major or delayed complications. There were 6 cases (2.8%) of minor complications, which included 2 cases (0.9%) with symptomatic hematomas and 4 cases (1.9%) with asymptomatic small hematomas. Conclusion: The findings confirm that CNB is effective in reducing the rate of inconclusive results and it is safe. CNB may be used as an alternative first-line diagnostic method for thyroid nodules by an experienced operator.
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Affiliation(s)
- Min Ji Hong
- Department of Radiology, Chung-Ang University College of Medicine, Chung-Ang University Hospital, Seoul, Korea
| | - Dong Gyu Na
- Department of Radiology, University of Ulsan College of Medicine, Gangneung Asan Hospital, Gangneung, Korea
- Department of Radiology, Human Medical Imaging and Intervention Center, Seoul, Korea
| | - Hunkyung Lee
- Department of Pathology, Ewha Clinical Laboratory, Seoul, Korea
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29
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Hahn SY, Shin JH, Oh YL, Park KW. Ultrasound-Guided Core Needle Biopsy Techniques for Intermediate or Low Suspicion Thyroid Nodules: Which Method is Effective for Diagnosis? Korean J Radiol 2020; 20:1454-1461. [PMID: 31544370 PMCID: PMC6757004 DOI: 10.3348/kjr.2018.0841] [Citation(s) in RCA: 6] [Impact Index Per Article: 1.2] [Reference Citation Analysis] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 11/30/2018] [Accepted: 06/18/2019] [Indexed: 11/18/2022] Open
Affiliation(s)
- Soo Yeon Hahn
- Department of Radiology and Center for Imaging Science, Thyroid Center, Samsung Medical Center, Sungkyunkwan University School of Medicine, Seoul, Korea
| | - Jung Hee Shin
- Department of Radiology and Center for Imaging Science, Thyroid Center, Samsung Medical Center, Sungkyunkwan University School of Medicine, Seoul, Korea.
| | - Young Lyun Oh
- Department of Pathology, Thyroid Center, Samsung Medical Center, Sungkyunkwan University School of Medicine, Seoul, Korea
| | - Ko Woon Park
- Department of Radiology and Center for Imaging Science, Thyroid Center, Samsung Medical Center, Sungkyunkwan University School of Medicine, Seoul, Korea
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30
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Ahn SH. Usage and Diagnostic Yield of Fine-Needle Aspiration Cytology and Core Needle Biopsy in Thyroid Nodules: A Systematic Review and Meta-Analysis of Literature Published by Korean Authors. Clin Exp Otorhinolaryngol 2020; 14:116-130. [PMID: 32550723 PMCID: PMC7904437 DOI: 10.21053/ceo.2020.00199] [Citation(s) in RCA: 3] [Impact Index Per Article: 0.6] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 02/12/2020] [Accepted: 03/19/2020] [Indexed: 11/25/2022] Open
Abstract
Objectives The usefulness of core needle biopsy (CNB) for the diagnosis of thyroid nodules remains controversial, and preferences vary across hospitals. The purpose of this study was to assess the actual use of CNB in Korea and to analyze the advantages and disadvantages of CNB through a systematic review and meta-analysis of papers published by Korean authors. Methods A meta-analysis of full-text publications published in English presenting data from Korea retrieved from the Embase literature database was performed. Results CNB led to a significantly lower proportion of non-diagnostic results than fine-needle aspiration (FNA). However, the frequency of atypia of undetermined significance/follicular lesion of undetermined significance (AUS/FLUS) did not decrease as a result of performing CNB in nodules with initial AUS/FLUS results, while it increased in consecutive cases. A subcategory analysis of AUS/FLUS showed that the increased frequency of AUS/FLUS findings on CNB was due to more frequent diagnoses of architectural atypia and follicular neoplasm, which resulted in a higher frequency of inconclusive findings in consecutive cases compared to FNA. Hospitals favoring CNB had a higher proportion of AUS/FLUS diagnoses. Although the complication rate did not differ significantly between CNB and FNA, serious complications of CNB did occur. Conclusion A reduced frequency of non-diagnostic results may be a definite advantage of CNB over FNA. However, the increased frequency of diagnoses of architectural atypia and follicular neoplasm should be considered when selecting CNB as a diagnostic tool.
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Affiliation(s)
- Soon-Hyun Ahn
- Department of Otorhinolaryngology-Head and Neck Surgery, Seoul National University Hospital, Seoul National University College of Medicine, Seoul, Korea
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31
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Ha SM, Baek JH, Na DG, Jung CK, Suh CH, Shong YK, Sung TY, Song DE, Lee JH. Assessing the diagnostic performance of thyroid biopsy with recommendations for appropriate interpretation. Ultrasonography 2020; 40:228-236. [PMID: 32660199 PMCID: PMC7994740 DOI: 10.14366/usg.19099] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 12/31/2019] [Accepted: 05/19/2020] [Indexed: 11/29/2022] Open
Abstract
Purpose The diagnostic performance of thyroid biopsy is influenced by several factors, including differences in the Bethesda categorization for malignancy, the inclusion or exclusion of non-diagnostic results, the definition used for the final diagnosis, and the definition of an inconclusive diagnosis. The purpose of this study was to provide an understanding of the factors influencing the diagnostic performance of thyroid biopsy. Methods We collected data retrospectively between January and December 2013 from a cohort of 6,762 thyroid nodules from 6,493 consecutive patients who underwent biopsy. In total, 4,822 nodules from 4,553 patients were included. We calculated the biopsy sensitivity according to the inclusion of different Bethesda categories in the numerator and the exclusion of non-diagnostic results, as well as the diagnostic accuracy according to different definitions of a benign diagnosis. We obtained the conclusive and inconclusive diagnosis rates. Results The sensitivity increased when more Bethesda categories were included in the numerator and when non-diagnostic results were excluded. When a benign thyroid nodule diagnosis was defined as benign findings on surgical resection, concordant benign results on at least two occasions, or an initial benign biopsy result and follow-up for more than 12 months, the accuracy was higher than when the diagnosis was based on surgical resection alone (91.1% vs. 68.7%). A higher conclusive diagnosis rate was obtained when Bethesda categories I and III were considered inconclusive than when Bethesda categories I, III and IV were considered inconclusive (78.3% vs. 72.8%, P<0.001). Conclusion Understanding the concepts presented herein is important in order to appropriately interpret the diagnostic performance of thyroid biopsy.
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Affiliation(s)
- Su Min Ha
- Department of Radiology and Thyroid Center, Chung-Ang University Hospital, Chung-Ang University College of Medicine, Seoul, Korea.,Department of Radiology and Research Institute of Radiology, Seoul National University Hospital, Seoul, Korea
| | - Jung Hwan Baek
- Department of Radiology and the Research Institute of Radiology, Asan Medical Center, University of Ulsan College of Medicine, Seoul, Korea
| | - Dong Gyu Na
- Department of Radiology, GangNeung Asan Hospital, Gangneung, Korea
| | - Chan-Kwon Jung
- Department of Pathology, Seoul St. Mary's Hospital, College of Medicine, The Catholic University of Korea, Seoul, Korea
| | - Chong Hyun Suh
- Department of Radiology and the Research Institute of Radiology, Asan Medical Center, University of Ulsan College of Medicine, Seoul, Korea
| | - Young Kee Shong
- Department of Internal Medicine, Asan Medical Center, University of Ulsan College of Medicine, Seoul, Korea
| | - Tae Yon Sung
- Department of Surgery, Asan Medical Center, University of Ulsan College of Medicine, Seoul, Korea
| | - Dong Eun Song
- Department of Pathology, Asan Medical Center, University of Ulsan College of Medicine, Seoul, Korea
| | - Jeong Hyun Lee
- Department of Radiology and the Research Institute of Radiology, Asan Medical Center, University of Ulsan College of Medicine, Seoul, Korea
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Park KW, Shin JH, Hahn SY, Oh YL, Kim SW, Kim TH, Chung JH. Ultrasound-guided fine-needle aspiration or core needle biopsy for diagnosing follicular thyroid carcinoma? Clin Endocrinol (Oxf) 2020; 92:468-474. [PMID: 32012326 DOI: 10.1111/cen.14167] [Citation(s) in RCA: 12] [Impact Index Per Article: 2.4] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 11/12/2019] [Revised: 01/29/2020] [Accepted: 02/01/2020] [Indexed: 12/21/2022]
Abstract
OBJECTIVE We evaluated the preoperative diagnostic values of ultrasound (US), fine-needle aspiration (FNA) and core needle biopsy (CNB) leading to surgery in patients with FTC. METHODS From October 1994 to July 2016, 298 patients with FTC who had preoperative US images and underwent US-guided FNA or CNB and surgery were included in this study. We evaluated the results of preoperative FNA or CNB based on the Bethesda system and the US findings according to the Korean thyroid imaging reporting and data system (K-TIRADS). RESULTS Predominant US features of FTC showed solid, hypo- or iso-echogenicity, oval smooth margin and halo with no calcification. Based on K-TIRADS, 140 (47.0%) patients with FTC were categorized as low suspicion, 133 (44.63%) as intermediate suspicion and 25 (8.4%) as high suspicion at US. Considering only FNA cytology (n = 230), 6.9% were revealed as Bethesda class I, 16.1% as class II, 37.0% as class III, 29.1% as class IV and 10.9% as class V. Considering the 68 cases with CNB results, 2.9% were revealed as class I, 4.4% as class II, 20.6% as class III and 72.1% as class IV. Despite multiple FNAs, 16.7% of the 84 patients with FTC still obtained Bethesda class I or class II. CNB results in patients with FTC had a significantly higher rate of Bethesda class IV compared to the FNA results (P < .001). FTCs with distant metastasis exhibited a significantly higher rate of Bethesda classes IV and V compared to those without distant metastasis (P = .004). CONCLUSION Surgery for FTC is deferred only with preoperative US and FNA. CNB in patients with FTC can lead to surgery better than FNA. Therefore, if the US feature is characteristic and a serially growing large nodule is suspected, the first attempt of CNB may be helpful in selecting a surgical candidate.
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Affiliation(s)
- Ko Woon Park
- Department of Radiology, Samsung Medical Center, Sungkyunkwan University School of Medicine, Seoul, Korea
| | - Jung Hee Shin
- Department of Radiology, Samsung Medical Center, Sungkyunkwan University School of Medicine, Seoul, Korea
| | - Soo Yeon Hahn
- Department of Radiology, Samsung Medical Center, Sungkyunkwan University School of Medicine, Seoul, Korea
| | - Young Lyun Oh
- Department of Pathology, Samsung Medical Center, Sungkyunkwan University School of Medicine, Seoul, Korea
| | - Sun Wook Kim
- Division of Endocrinology and Metabolism, Department of Medicine, Samsung Medical Center, Sungkyunkwan University School of Medicine, Seoul, Korea
| | - Tae Hyuk Kim
- Division of Endocrinology and Metabolism, Department of Medicine, Samsung Medical Center, Sungkyunkwan University School of Medicine, Seoul, Korea
| | - Jae Hoon Chung
- Division of Endocrinology and Metabolism, Department of Medicine, Samsung Medical Center, Sungkyunkwan University School of Medicine, Seoul, Korea
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Chung SR, Baek JH, Choi YJ, Sung TY, Song DE, Kim TY, Lee JH. The relationship of thyroid nodule size on malignancy risk according to histological type of thyroid cancer. Acta Radiol 2020; 61:620-628. [PMID: 31554409 DOI: 10.1177/0284185119875642] [Citation(s) in RCA: 5] [Impact Index Per Article: 1.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 01/07/2023]
Abstract
Background Although several studies have examined the value of thyroid nodule size as a malignancy predictor, the results are conflicting. Purpose To investigate the relationship between nodule size and malignancy risk and to evaluate the impact of nodule size on the false-negative rate of fine needle aspiration or core needle biopsy according to the histological type of thyroid cancer. Material and Methods From January 2013 to December 2013, 3970 thyroid nodules that underwent ultrasound-guided fine needle aspiration or core needle biopsy were retrospectively reviewed. We assessed the relationship between nodule size and malignancy risk according to histological type of thyroid cancer. In addition, we compared the false-negative rate by thyroid nodule size category. Results Of 3970 thyroid nodules, 1170 nodules were malignant. For papillary thyroid carcinoma, nodule size was inversely related to malignancy risk, whereas in nodules of follicular carcinoma and follicular variant papillary thyroid carcinoma, nodule size was positively related to malignancy risk ( P < 0.001). The false-negative rate tended to increase as nodule size increased ( P = 0.002) for all nodules and the overall false-negative rate was 2.3%. Conclusion Overall, nodule size does not correlate with risk of malignancy, but the relationship between nodule size and malignancy risk depends on the histological type of thyroid cancer.
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Affiliation(s)
- Sae Rom Chung
- Department of Radiology and the Research Institute of Radiology, University of Ulsan College of Medicine, Asan Medical Center, Seoul, Republic of Korea
| | - Jung Hwan Baek
- Department of Radiology and the Research Institute of Radiology, University of Ulsan College of Medicine, Asan Medical Center, Seoul, Republic of Korea
| | - Young Jun Choi
- Department of Radiology and the Research Institute of Radiology, University of Ulsan College of Medicine, Asan Medical Center, Seoul, Republic of Korea
| | - Tae-Yon Sung
- Department of Surgery, University of Ulsan College of Medicine, Asan Medical Center, Seoul, Republic of Korea
| | - Dong Eun Song
- Department of Pathology, University of Ulsan College of Medicine, Asan Medical Center, Seoul, Republic of Korea
| | - Tae Yong Kim
- Department of Endocrinology and Metabolism, University of Ulsan College of Medicine, Asan Medical Center, Seoul, Republic of Korea
| | - Jeong Hyun Lee
- Department of Radiology and the Research Institute of Radiology, University of Ulsan College of Medicine, Asan Medical Center, Seoul, Republic of Korea
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Sohn YM, Na DG, Paik W, Gwon HY, Noh BJ. Malignancy risk of thyroid nodules with nonshadowing echogenic foci. Ultrasonography 2020; 40:115-125. [PMID: 32594667 PMCID: PMC7758109 DOI: 10.14366/usg.20012] [Citation(s) in RCA: 4] [Impact Index Per Article: 0.8] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/29/2020] [Accepted: 04/19/2020] [Indexed: 11/30/2022] Open
Abstract
Purpose This study was conducted to determine the malignancy risk and diagnostic value of various types of nonshadowing echogenic foci (NEF) in the risk stratification of thyroid nodules. Methods A total of 1,018 consecutive thyroid nodules (≥1 cm) with final diagnoses were included. The presence of NEF was determined and types of NEF were classified according to the presence of a comet tail artifact (CTA), location, and size through a prospective evaluation. The associations with malignancy, malignancy risk, and diagnostic value of various types of NEF were assessed. Results Intrasolid punctate NEF without CTA was the only type of NEF that was an independent predictor of malignancy (P<0.001). The malignancy risk of intrasolid punctate NEF without CTA was substantially higher in solid hypoechoic nodules than in isoechoic or nonsolid nodules (71.3% vs. 9.2%, P<0.001). In solid hypoechoic nodules, slightly increased sensitivity (70.8% vs. 67.9%) for malignancy and a similar malignancy risk (71.4% vs. 71.3%) were observed for intrasolid punctate NEF (with or without CTA) and intrasolid punctate NEF without CTA, respectively. NEF with CTA at the margin of the cystic component was not associated with malignancy or benignity in nonsolid nodules (P>0.05). Conclusion Intrasolid punctate NEF without CTA was the only independent predictor of malignancy. However, solid hypoechoic nodules with intrasolid punctate NEF should be classified as high-suspicion nodules regardless of coexisting CTA. Other types of NEF had no added value for detecting malignancy compared to intrasolid punctate NEF without CTA.
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Affiliation(s)
- Yu-Mee Sohn
- Department of Radiology, Kyung Hee University Hospital, Kyung Hee University College of Medicine, Seoul, Korea
| | - Dong Gyu Na
- Department of Radiology, Gangneung Asan Hospital, University of Ulsan College of Medicine, Gangneung, Korea
| | - Wooyul Paik
- Department of Radiology, Gangneung Asan Hospital, University of Ulsan College of Medicine, Gangneung, Korea
| | - Hye Yun Gwon
- Department of Radiology, Gangneung Asan Hospital, University of Ulsan College of Medicine, Gangneung, Korea
| | - Byeong-Joo Noh
- Department of Pathology, Gangneung Asan Hospital, University of Ulsan College of Medicine, Gangneung, Korea
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Hahn SY, Shin JH, Oh YL, Park KW, Lim Y. Comparison Between Fine Needle Aspiration and Core Needle Biopsy for the Diagnosis of Thyroid Nodules: Effective Indications According to US Findings. Sci Rep 2020; 10:4969. [PMID: 32188891 PMCID: PMC7080804 DOI: 10.1038/s41598-020-60872-z] [Citation(s) in RCA: 13] [Impact Index Per Article: 2.6] [Reference Citation Analysis] [Abstract] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/12/2019] [Accepted: 02/13/2020] [Indexed: 01/25/2023] Open
Abstract
Thyroid nodules are initially handled by fine needle aspiration (FNA). However, the stance of thyroid core needle biopsy (CNB) still is a challenge. This study aimed to compare the diagnostic performances and conclusive rates of FNA and CNB for the diagnosis of thyroid nodules and to define effective indications of CNB. This retrospective study enrolled 1,060 consecutive thyroid nodules in 1,037 patients who underwent FNA from January 2008 to May 2008, and 462 consecutive nodules in 453 patients who underwent CNB from January 2014 to December 2015 at our institution. Ultrasound (US) features were classified according to the American College of Radiology Thyroid Imaging Reporting and Data System (ACR TI-RADS) and Korean TIRADS (K-TIRADS). We compared diagnostic performances and conclusive rates between FNA and CNB groups. Propensity score matching was conducted to match FNA patients with CNB patients. After matching, the diagnostic performances for selecting surgical candidates and predicting malignancy were comparable between the two biopsy groups. Based on US findings, conclusive results were obtained significantly more in CNB than in FNA when thyroid nodules were classified as ACR TI-RADS or K-TIRADS category 4 and measured larger than 2 cm. Diagnostic performances between FNA and CNB were comparable. Superiority of CNB to FNA was found for thyroid nodules larger than 2 cm and classified as ACR TI-RADS or K-TIRADS category 4.
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Affiliation(s)
- Soo Yeon Hahn
- Department of Radiology and Center for Imaging Science, Samsung Medical Center, Sungkyunkwan University School of Medicine, 81 Irwon-ro, Gangnam-gu, Seoul, 06351, Republic of Korea
| | - Jung Hee Shin
- Department of Radiology and Center for Imaging Science, Samsung Medical Center, Sungkyunkwan University School of Medicine, 81 Irwon-ro, Gangnam-gu, Seoul, 06351, Republic of Korea.
| | - Young Lyun Oh
- Department of Pathology, Samsung Medical Center, Sungkyunkwan University School of Medicine, 81 Irwon-ro, Gangnam-gu, Seoul, 06351, Republic of Korea
| | - Ko Woon Park
- Department of Radiology and Center for Imaging Science, Samsung Medical Center, Sungkyunkwan University School of Medicine, 81 Irwon-ro, Gangnam-gu, Seoul, 06351, Republic of Korea
| | - Yaeji Lim
- Department of Applied Statistics, Chung-Ang University, 84, Heukseok-ro, Dongjak-gu, Seoul, 06974, Republic of Korea
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Kim NR, Seok JY, Chung YS, Lee JH, Chung DH. Contribution of cytologic examination to diagnosis of poorly differentiated thyroid carcinoma. J Pathol Transl Med 2020; 54:171-178. [PMID: 32013325 PMCID: PMC7093280 DOI: 10.4132/jptm.2019.12.03] [Citation(s) in RCA: 4] [Impact Index Per Article: 0.8] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 08/09/2019] [Accepted: 12/03/2019] [Indexed: 12/02/2022] Open
Abstract
Background The cytologic diagnosis of poorly differentiated thyroid carcinoma (PDTC) is difficult because it lacks salient cytologic findings and shares cytologic features with more commonly encountered neoplasms. Due to diverse cytologic findings and paucicellularity of PDTC, standardization of cytologic diagnostic criteria is limited. The purpose of this study is to investigate and recognize diverse thyroid findings of fine needle aspiration (FNA) cytology and frozen smear cytology in diagnosis of this rare but aggressive carcinoma. Methods The present study included six cases of FNA cytology and frozen smears of histologically diagnosed PDTCs. Results PDTC showed cytologic overlap with well-differentiated thyroid carcinomas (WDTCs). Five of six cases showed dedifferentiation arising from well differentiated thyroid carcinomas. Only one de novo PDTC showed highly cellular smears composed of discohesive small cells, high nuclear/cytoplasmic (N/C) ratio, prominent micronucleoli, and irregular nuclei. Retrospectively reviewed, these findings are highly suspicious for PDTC. Cytologic findings of nuclear atypia, pleomorphism, and irregularity were frequently found, whereas scattered small cells were seen only in the de novo case. Conclusions Heterogeneous cytologic findings of PDTCs are shared with those of WDTCs and contribute to difficult preoperative cytologic diagnoses. Most PDTCs show dedifferentiation from WDTCs. Albeit rare, de novo PDTC should be considered with cytology showing discohesive small cells with high N/C ratio. This will enable precise diagnosis and prompt treatment of this aggressive malignancy
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Affiliation(s)
- Na Rae Kim
- Department of Pathology, Gil Medical Center, Gachon University College of Medicine, Incheon, Korea
| | - Jae Yeon Seok
- Department of Pathology, Gil Medical Center, Gachon University College of Medicine, Incheon, Korea
| | - Yoo Seung Chung
- Division of Thyroid Clinic, Department of General Surgery, Gil Medical Center, Gachon University College of Medicine, Incheon, Korea
| | - Joon Hyop Lee
- Division of Thyroid Clinic, Department of General Surgery, Gil Medical Center, Gachon University College of Medicine, Incheon, Korea
| | - Dong Hae Chung
- Department of Pathology, Gil Medical Center, Gachon University College of Medicine, Incheon, Korea
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Shin I, Kim EK, Moon HJ, Yoon JH, Park VY, Lee SE, Lee HS, Kwak JY. Core-Needle Biopsy Does Not Show Superior Diagnostic Performance to Fine-Needle Aspiration for Diagnosing Thyroid Nodules. Yonsei Med J 2020; 61:161-168. [PMID: 31997625 PMCID: PMC6992459 DOI: 10.3349/ymj.2020.61.2.161] [Citation(s) in RCA: 5] [Impact Index Per Article: 1.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 11/22/2019] [Revised: 12/24/2019] [Accepted: 12/24/2019] [Indexed: 12/16/2022] Open
Abstract
PURPOSE To compare the diagnostic performances of fine-needle aspiration (FNA) and core-needle biopsy (CNB) for thyroid nodules according to nodule size. MATERIALS AND METHODS This retrospective study included 320 thyroid nodules from 320 patients who underwent both FNA and CNB at outside clinics and proceeded with surgery in our institution between July 2012 and May 2019. According to nodule size, the diagnostic performances of FNA and CNB were calculated using various combinations of test-negatives and test-positives defined by the Bethesda categories and were compared using the generalized estimated equation and the Delong method. RESULTS There were 279 malignant nodules in 279 patients and 41 benign nodules in 41 patients. The diagnostic performance of FNA was mostly not different from CNB regardless of nodule size, except for negative predictive value, which was better for FNA than CNB when applying Criteria 1 and 2. When applying Criteria 3, the specificity and positive predictive value of FNA were superior to CNB regardless of size. When applying Criteria 4, diagnostic performance did not differ between FNA and CNB regardless of size. After applying Criteria 5, diagnostic performance did not differ between FNA and CNB in nodules ≥2 cm. However, in nodules ≥1 cm and all nodules, the sensitivity, accuracy, and negative predictive value of CNB were better than those of FNA. CONCLUSION CNB did not show superior diagnostic performance to FNA for diagnosing thyroid nodules.
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Affiliation(s)
- Ilah Shin
- Department of Radiology, Severance Hospital, Research Institute of Radiological Science, Yonsei University College of Medicine, Seoul, Korea
| | - Eun Kyung Kim
- Department of Radiology, Severance Hospital, Research Institute of Radiological Science, Yonsei University College of Medicine, Seoul, Korea
| | - Hee Jung Moon
- Department of Radiology, Severance Hospital, Research Institute of Radiological Science, Yonsei University College of Medicine, Seoul, Korea
| | - Jung Hyun Yoon
- Department of Radiology, Severance Hospital, Research Institute of Radiological Science, Yonsei University College of Medicine, Seoul, Korea
| | - Vivian Youngjean Park
- Department of Radiology, Severance Hospital, Research Institute of Radiological Science, Yonsei University College of Medicine, Seoul, Korea
| | - Si Eun Lee
- Department of Radiology, Severance Hospital, Research Institute of Radiological Science, Yonsei University College of Medicine, Seoul, Korea
| | - Hye Sun Lee
- Biostatistics Collaboration Unit, Yonsei University College of Medicine, Seoul, Korea
| | - Jin Young Kwak
- Department of Radiology, Severance Hospital, Research Institute of Radiological Science, Yonsei University College of Medicine, Seoul, Korea.
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Son HM, Kim JH, Kim SC, Yoo RE, Bae JM, Seo H, Na DG. Distribution and malignancy risk of six categories of the pathology reporting system for thyroid core-needle biopsy in 1,216 consecutive thyroid nodules. Ultrasonography 2020; 39:159-165. [PMID: 32105436 PMCID: PMC7065982 DOI: 10.14366/usg.19056] [Citation(s) in RCA: 9] [Impact Index Per Article: 1.8] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/10/2019] [Accepted: 01/16/2020] [Indexed: 12/14/2022] Open
Abstract
PURPOSE The purpose of this study was to present the distribution of lesions among the six categories of the pathology reporting system for thyroid core-needle biopsy (CNB), along with the range of malignancy risk of each category based on different diagnostic criteria for benignity in a clinical cohort. METHODS For 1,216 consecutive nodules (≥1 cm) of 1,125 patients who underwent CNB at two hospitals, the diagnostic results based on the six categories of thyroid CNB were analyzed. Patients were divided into three groups according to prior fine-needle aspiration (FNA) status: second-line CNB for nodules where prior FNA yielded nondiagnostic or unsatisfactory results (n=57), second-line CNB for nodules with prior FNA results of atypia/follicular lesion of undetermined significance (AUS/FLUS) (n=303), and first-line CNB (n=856). RESULTS The proportion of nodules in each CNB category and the range of the malignancy rate for each category was as follows, in order from category I to VI: 1.8%, 23.1%-75.0%; 57.9%, 0.7%-16.7%; 16.0%, 13.2%-46.7%; 8.8%, 53.8%-56.8%; 2.0%, 100%; and 13.5%, 100%. First-line CNB was associated with a higher rate of conclusive diagnoses (category II, IV, or VI) (725 of 856, 84.7%) than second-line CNB with prior nondiagnostic or AUS/FLUS FNA results (241 of 360, 66.9%; P<0.001). CONCLUSION The overall distribution of nodules across the six categories of thyroid CNB and the ranges of malignancy risk for those categories were presented in a clinical cohort. First-line CNB tended to produce a higher rate of conclusive results than second-line CNB with prior inconclusive FNA results.
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Affiliation(s)
- Hye Min Son
- Department of Radiology, Seoul National University Hospital, Seoul, Korea.,Department of Radiology, Yeungnam University College of Medicine, Daegu, Korea
| | - Ji-Hoon Kim
- Department of Radiology, Seoul National University Hospital, Seoul, Korea
| | - Soo Chin Kim
- Department of Radiology, Seoul National University Hospital Healthcare System Gangnam Center, Seoul, Korea
| | - Roh-Eul Yoo
- Department of Radiology, Seoul National University Hospital, Seoul, Korea
| | - Jeong Mo Bae
- Department of Pathology, Seoul National University Hospital, Seoul, Korea
| | - Hyobin Seo
- Department of Radiology, Seoul National University Hospital Healthcare System Gangnam Center, Seoul, Korea.,Department of Radiology, Human Medical Imaging and Intervention Center, Seoul, Korea
| | - Dong Gyu Na
- Department of Radiology, Human Medical Imaging and Intervention Center, Seoul, Korea.,Department of Radiology, GangNeung Asan Hospital, Gangneung, Korea
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Jung CK, Baek JH, Na DG, Oh YL, Yi KH, Kang HC. 2019 Practice guidelines for thyroid core needle biopsy: a report of the Clinical Practice Guidelines Development Committee of the Korean Thyroid Association. J Pathol Transl Med 2020; 54:64-86. [PMID: 31964112 PMCID: PMC6986975 DOI: 10.4132/jptm.2019.12.04] [Citation(s) in RCA: 30] [Impact Index Per Article: 6.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 11/21/2019] [Accepted: 12/04/2019] [Indexed: 12/31/2022] Open
Abstract
Ultrasound-guided core needle biopsy (CNB) has been increasingly used for the pre-operative diagnosis of thyroid nodules. Since the Korean Society of the Thyroid Radiology published the ‘Consensus Statement and Recommendations for Thyroid CNB’ in 2017 and the Korean Endocrine Pathology Thyroid CNB Study Group published ‘Pathology Reporting of Thyroid Core Needle Biopsy’ in 2015, advances have occurred rapidly not only in the management guidelines for thyroid nodules but also in the diagnostic terminology and classification schemes. The Clinical Practice Guidelines Development Committee of the Korean Thyroid Association (KTA) reviewed publications on thyroid CNB from 1995 to September 2019 and updated the recommendations and statements for the diagnosis and management of thyroid nodules using CNB. Recommendations for the resolution of clinical controversies regarding the use of CNB were based on expert opinion. These practical guidelines include recommendations and statements regarding indications for CNB, patient preparation, CNB technique, biopsy-related complications, biopsy specimen preparation and processing, and pathology interpretation and reporting of thyroid CNB.
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Affiliation(s)
- Chan Kwon Jung
- Department of Hospital Pathology, College of Medicine, The Catholic University of Korea, Seoul, Korea.,Cancer Research Institute, College of Medicine, The Catholic University of Korea, Seoul, Korea
| | - Jung Hwan Baek
- Department of Radiology and Research Institute of Radiology, Asan Medical Center, University of Ulsan College of Medicine, Seoul, Korea
| | - Dong Gyu Na
- Department of Radiology, Gangneung Asan Hospital, University of Ulsan College of Medicine, Gangneung, Korea
| | - Young Lyun Oh
- Department of Pathology and Translational Genomics, Samsung Medical Center, Sungkyunkwan University School of Medicine, Seoul, Korea
| | - Ka Hee Yi
- Department of Internal Medicine, Seoul Metropolitan Government Seoul National University Boramae Medical Center, Seoul, Korea
| | - Ho-Cheol Kang
- Department of Internal Medicine, Chonnam National University Hwasun Hospital, Chonnam National University Medical School, Hwasun, Korea
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Na HY, Woo JW, Moon JH, Choi JY, Jeong WJ, Kim YK, Choe JY, Park SY. Preoperative Diagnostic Categories of Noninvasive Follicular Thyroid Neoplasm with Papillary-Like Nuclear Features in Thyroid Core Needle Biopsy and Its Impact on Risk of Malignancy. Endocr Pathol 2019; 30:329-339. [PMID: 31605276 DOI: 10.1007/s12022-019-09590-5] [Citation(s) in RCA: 3] [Impact Index Per Article: 0.5] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Indexed: 01/21/2023]
Abstract
This study was designed to evaluate the preoperative diagnostic categories of noninvasive follicular thyroid neoplasm with papillary-like nuclear features (NIFTP) using thyroid core needle biopsy (CNB) and to analyze its impact on the risk of malignancy (ROM). A total of 2687 consecutive thyroid CNBs were reviewed retrospectively and classified into six diagnostic categories using a standardized reporting system similar to the Bethesda System for Reporting Thyroid Cytopathology. Diagnostic categories of CNBs were compared with the final surgical diagnoses, and the ROM in each category was calculated both before and after excluding NIFTP from malignancy. Of 946 surgically resected cases, 683 were diagnosed as papillary thyroid carcinoma (PTC), and 32 (4.7% of PTC) were reclassified as NIFTP. The CNB diagnostic categories of NIFTP were as follows: follicular neoplasm in 20 (62.5%; 14, with nuclear atypia), indeterminate lesion in 11 (34.4%), and suspicious for malignancy in one (3.1%). When combined, NIFTP and encapsulated follicular variant of PTC (EFVPTC) were more often categorized as follicular neoplasm compared with other PTC variants including infiltrative FVPTC. Exclusion of NIFTP from malignant diagnosis led to a significant decrease in the ROM in follicular neoplasm with nuclear atypia category. Thus, thyroid CNB enables to differentiate NIFTP/EFVPTC from other PTCs, providing a useful guide for optimal treatment in patients with these tumors.
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Affiliation(s)
- Hee Young Na
- Department of Pathology, Seoul National University Bundang Hospital, Seoul National University College of Medicine, 82, Gumi-ro 173 Beon-gil, Bundang-gu, Seongnam, Gyeonggi, 13620, Republic of Korea
| | - Ji Won Woo
- Department of Pathology, Seoul National University Bundang Hospital, Seoul National University College of Medicine, 82, Gumi-ro 173 Beon-gil, Bundang-gu, Seongnam, Gyeonggi, 13620, Republic of Korea
| | - Jae Hoon Moon
- Department of Internal Medicine, Seoul National University Bundang Hospital, Seoul National University College of Medicine, Seongnam, Gyeonggi, Republic of Korea
| | - June Young Choi
- Department of Surgery, Seoul National University Bundang Hospital, Seoul National University College of Medicine, Seongnam, Gyeonggi, Republic of Korea
| | - Woo-Jin Jeong
- Department of Otorhinolaryngology-Head and Neck Surgery, Seoul National University Bundang Hospital, Seoul National University College of Medicine, Seongnam, Gyeonggi, Republic of Korea
| | - Yeo Koon Kim
- Department of Radiology, Seoul National University Bundang Hospital, Seoul National University College of Medicine, Seongnam, Gyeonggi, Republic of Korea
| | - Ji-Young Choe
- Department of Pathology, Hallym University Sacred Heart Hospital, Anyang, Gyeonggi, Republic of Korea
| | - So Yeon Park
- Department of Pathology, Seoul National University Bundang Hospital, Seoul National University College of Medicine, 82, Gumi-ro 173 Beon-gil, Bundang-gu, Seongnam, Gyeonggi, 13620, Republic of Korea.
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Paik W, Na DG, Gwon HY, Kim J. CT features of thyroid nodules with isolated macrocalcifications detected by ultrasonography. Ultrasonography 2019; 39:130-136. [PMID: 31962383 PMCID: PMC7065983 DOI: 10.14366/usg.19045] [Citation(s) in RCA: 8] [Impact Index Per Article: 1.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 08/15/2019] [Accepted: 10/23/2019] [Indexed: 12/18/2022] Open
Abstract
Purpose A thyroid nodule with an isolated macrocalcification is visualized as a calcified nodule with complete posterior shadowing on ultrasonography (US). This study aimed to determine the computed tomography (CT) features of isolated macrocalcifications detected using US. Methods This study included 20 patients who had thyroid nodules with isolated macroalcifications and underwent neck CT or chest CT. The patients were enrolled from a sample of 82 patients with isolated macrocalcifications detected by US drawn from 7,142 consecutive patients who underwent thyroid biopsy at two institutions. We evaluated the CT features of nodules with isolated macrocalcifications and categorized them as central or rim calcifications. We assessed the nodule size and the frequency of nondiagnostic fine-needle aspiration (FNA) results and malignant tumors according to the CT features of isolated macrocalcifications. Results CT scans showed central calcifications in 18 (90.0%) and rim calcifications in two (10.0%) of the 20 nodules with isolated macrocalcifications. Among the 18 nodules with central isolated macrocalcifications, complete compact calcification was found in six nodules and partial coarse calcification in 12 nodules. In 18 nodules with central isolated macrocalcifications, the nondiagnostic FNA rate and frequency of malignant tumors were not significantly different between complete and partial central calcifications (P=0.620 and P=0.999, respectively). Malignant tumors were only found in nodules with central isolated macrocalcifications. Conclusion The majority of nodules with isolated macrocalcifications showed central calcifications on CT. Thyroid nodules with isolated macrocalcifications detected by US should not be classified as having a type of rim or peripheral calcification.
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Affiliation(s)
- Wooyul Paik
- Department of Radiology, Gangneung Asan Hospital, University of Ulsan College of Medicine, Gangneung, Korea
| | - Dong Gyu Na
- Department of Radiology, Gangneung Asan Hospital, University of Ulsan College of Medicine, Gangneung, Korea.,Department of Radiology, Human Medical Imaging and Intervention Center, Seoul, Korea
| | - Hye Yun Gwon
- Department of Radiology, Gangneung Asan Hospital, University of Ulsan College of Medicine, Gangneung, Korea
| | - Jinna Kim
- Department of Radiology, Yonsei University College of Medicine, Seoul, Korea
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Jin Kim H, Koon Kim Y, Hoon Moon J, Young Choi J, Il Choi S. Thyroid core needle biopsy: patients' pain and satisfaction compared to fine needle aspiration. Endocrine 2019; 65:365-370. [PMID: 31203562 DOI: 10.1007/s12020-019-01973-2] [Citation(s) in RCA: 6] [Impact Index Per Article: 1.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 03/27/2019] [Accepted: 05/27/2019] [Indexed: 01/21/2023]
Abstract
PURPOSE The purpose of this study was to compare patients' pain and satisfaction of fine needle aspiration (FNA) and core needle biopsy (CNB) for a thyroid nodule. METHODS We consecutively enrolled patients with thyroid nodules who underwent ultrasound-guided FNA or CNB in our institution. The patients answered a questionnaire about pain scores during the procedure, immediately after the procedure and 20 min after the procedure, and any complication after the biopsy. Through a phone interview which was conducted 2 weeks after the procedure, a researcher asked the patients about residual pain and overall subjective satisfaction score about the procedures. Patients were also asked to report any complication or complaint after the procedures on the phone interview. RESULTS The 167 patients who had undergone thyroid FNA (n = 87) or CNB (n = 80) were included. The pain scores were not significantly different between the two groups during the procedure and after the procedure. Overall satisfaction scores after 2 weeks were not different, either. There was no acute or delayed major complication in both groups. CONCLUSIONS Differences regarding patients' pain and satisfaction scores between CNB and FNA were not demonstrated.
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Affiliation(s)
- Hyo Jin Kim
- Department of Radiology, SMG-SNU Boramae Medical Center, Seoul, South Korea
| | - Yeo Koon Kim
- Department of Radiology, Seoul National University Bundang Hospital, Seongnam, South Korea.
| | - Jae Hoon Moon
- Division of Endocrinology and Metabolism, Department of Internal Medicine, Seoul National University Bundang Hospital, Seongnam, South Korea
| | - June Young Choi
- Department of Surgery, Seoul National University Bundang Hospital, Seongnam, South Korea
| | - Sang Il Choi
- Department of Radiology, Seoul National University Bundang Hospital, Seongnam, South Korea
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Yim Y, Baek JH. Core needle biopsy in the management of thyroid nodules with an indeterminate fine-needle aspiration report. Gland Surg 2019; 8:S77-S85. [PMID: 31475094 DOI: 10.21037/gs.2018.09.07] [Citation(s) in RCA: 7] [Impact Index Per Article: 1.2] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 12/20/2022]
Abstract
Ultrasonography (US)-guided fine-needle aspiration biopsy (FNAB) cytology is widely used but is limited due to its pathologically indeterminate results in diagnosing thyroid nodules. Recently, US-guided core-needle biopsy (CNB) was introduced as an effective and safe technique for diagnosing indeterminate thyroid nodules. Using CNB, information about architectural histologic structure such as nodule capsule or more immunochemical staining can be obtained which lead to a more accurate diagnosis. Up to 98% of indeterminate thyroid lesions can be classified as malignant or benign when CNB is used for follow-up analysis. Other evidences revealed the effectiveness of CNB in reducing inconclusive results and improving the diagnostic performance of thyroid nodules initially diagnosed as AUS/FLUS by FNAB. In this review, we investigate how to deal with indeterminate thyroid nodules diagnosed by FNAB and determine how CNB has a role in diagnosing these indeterminate thyroid nodules.
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Affiliation(s)
- Younghee Yim
- Department of Radiology, Kangwon National University School of Medicine, Kangwon National University Hospital, Chuncheon, Korea
| | - Jung Hwan Baek
- Department of Radiology and Research Institute of Radiology, University of Ulsan College of Medicine, Asan Medical Center, Seoul, Korea
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Chung SR, Baek JH, Lee JH, Lee YM, Sung TY, Chung KW, Hong SJ, Jeon MJ, Kim TY, Shong YK, Kim WB, Kim WG, Song DE. Risk of Malignancy According to the Sub-classification of Atypia of Undetermined Significance and Suspicious Follicular Neoplasm Categories in Thyroid Core Needle Biopsies. Endocr Pathol 2019; 30:146-154. [PMID: 31044350 DOI: 10.1007/s12022-019-9577-4] [Citation(s) in RCA: 6] [Impact Index Per Article: 1.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Indexed: 01/16/2023]
Abstract
The objective of this study was to evaluate the risk of malignancy (ROM) associated with atypia of undetermined significance (AUS) and suspicious follicular neoplasm (SFN) core needle biopsy (CNB) categories after further sub-classification. Data from 2267 thyroid nodules evaluated by ultrasound-guided CNB, from January to December 2015, were retrospectively reviewed. AUS nodules (n = 556) were sub-classified as follows: (1) architectural atypia (AUS-A; n = 369, 66.4%), (2) cytologic atypia (AUS-C; n = 35, 6.3%), (3) cytologic/architectural atypia (AUS-C/A; n = 85, 15.3%), or (4) oncocytic atypia (AUS-O; n = 67, 12.1%). SFN nodules (n = 172) were sub-classified as follows: (1) architectural atypia only (SFN-A; n = 110, 64%), (2) cytologic/architectural atypia (SFN-C/A; n = 24, 14%), or (3) oncocytic atypia (SFN-O; n = 38, 22%). Diagnostic surgery was performed in 162 (30.2%) AUS cases and 105 (61%) SFN cases. The ROM of each sub-category was evaluated. The overall ROM was 15.3-52.5% in AUS nodules and 35.5-58.1% in SFN nodules. The ROM was higher in the AUS-C (22.9-88.9%) and AUS-C/A (32.9-90.3%) groups than AUS-A (11.9-40%) and AUS-O (7.5-41.7%). In the SFN category, ROM in the SFN-C/A group was also higher than SFN-A or SFN-O (37.5-75%, 40-57.9%, and 21.1-47.1%, respectively). Our study shows that the ROM was higher in AUS or SFN sub-categories with cytologic atypia than those without cytologic atypia. Because of the heterogeneous nature of AUS and SFN categories, sub-classification may be a more effective approach for risk stratification, allowing optimal management of patients with thyroid nodules.
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Affiliation(s)
- Sae Rom Chung
- Departments of Radiology Asan Medical Center, University of Ulsan College of Medicine, Seoul, 05505, South Korea
| | - Jung Hwan Baek
- Departments of Radiology Asan Medical Center, University of Ulsan College of Medicine, Seoul, 05505, South Korea
| | - Jeong Hyun Lee
- Departments of Radiology Asan Medical Center, University of Ulsan College of Medicine, Seoul, 05505, South Korea
| | - Yu-Mi Lee
- Departments of Surgery Asan Medical Center, University of Ulsan College of Medicine, Seoul, 05505, South Korea
| | - Tae-Yon Sung
- Departments of Surgery Asan Medical Center, University of Ulsan College of Medicine, Seoul, 05505, South Korea
| | - Ki-Wook Chung
- Departments of Surgery Asan Medical Center, University of Ulsan College of Medicine, Seoul, 05505, South Korea
| | - Suck Joon Hong
- Departments of Surgery Asan Medical Center, University of Ulsan College of Medicine, Seoul, 05505, South Korea
| | - Min Ji Jeon
- Departments of Internal Medicine Asan Medical Center, University of Ulsan College of Medicine, Seoul, 05505, South Korea
| | - Tae Yong Kim
- Departments of Internal Medicine Asan Medical Center, University of Ulsan College of Medicine, Seoul, 05505, South Korea
| | - Young Kee Shong
- Departments of Internal Medicine Asan Medical Center, University of Ulsan College of Medicine, Seoul, 05505, South Korea
| | - Won Bae Kim
- Departments of Internal Medicine Asan Medical Center, University of Ulsan College of Medicine, Seoul, 05505, South Korea
| | - Won Gu Kim
- Departments of Internal Medicine Asan Medical Center, University of Ulsan College of Medicine, Seoul, 05505, South Korea
| | - Dong Eun Song
- Departments of Pathology, Asan Medical Center, University of Ulsan College of Medicine, 88 Olympic-ro 43-gil, Songpa-gu, Seoul, 05505, South Korea.
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Ha SM, Shin JY, Baek JH, Song DE, Chung SR, Choi YJ, Lee JH. Does Radiofrequency Ablation Induce Neoplastic Changes in Benign Thyroid Nodules: A Preliminary Study. Endocrinol Metab (Seoul) 2019; 34:169-178. [PMID: 31099203 PMCID: PMC6599903 DOI: 10.3803/enm.2019.34.2.169] [Citation(s) in RCA: 26] [Impact Index Per Article: 4.3] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 01/03/2019] [Revised: 03/15/2019] [Accepted: 04/03/2019] [Indexed: 01/09/2023] Open
Abstract
BACKGROUND To evaluate the clinical feasibility of radiofrequency ablation (RFA) of benign thyroid nodules along with cytomorphological alteration, and any malignant transformation through biopsy. METHODS The data were retrospectively collected between April 2008 and June 2013 and core needle biopsy (CNB) was performed on 16 benign thyroid nodules previously treated using RFA. The parameters of the patients were compared, between the time of enrollment and the last follow-up examination, using linear mixed model statistical analysis. RESULTS No atypical cells or neoplastic transformation were detected in the undertreated peripheral portion of treated benign nodules on the CNB specimen. RFA altered neither the thyroid capsule nor the thyroid tissue adjacent to the treated area. On histopathological examinations, we observed 81.2% acellular hyalinization, which was the most common finding. After a mean follow-up period of over 5 years, the mean volume of thyroid nodule had decreased to 6.4±4.2 mL, with a reduction rate of 81.3%±5.8% (P<0.0001). CONCLUSION RFA is a technically feasible treatment method for benign thyroid nodules, with no carcinogenic effect or tissue damage of the normal thyroid tissue adjacent to the RFA-treated zone.
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Affiliation(s)
- Su Min Ha
- Department of Radiology, Seoul National University Hospital, Seoul National University College of Medicinee, Seoul, Korea
| | - Jun Young Shin
- Department of Pathology, Asan Medical Center, University of Ulsan College of Medicine, Seoul, Korea
| | - Jung Hwan Baek
- Department of Radiology and the Research Institute of Radiology, Asan Medical Center, University of Ulsan College of Medicine, Seoul, Korea
| | - Dong Eun Song
- Department of Pathology, Asan Medical Center, University of Ulsan College of Medicine, Seoul, Korea.
| | - Sae Rom Chung
- Department of Radiology and the Research Institute of Radiology, Asan Medical Center, University of Ulsan College of Medicine, Seoul, Korea
| | - Young Jun Choi
- Department of Radiology and the Research Institute of Radiology, Asan Medical Center, University of Ulsan College of Medicine, Seoul, Korea
| | - Jeong Hyun Lee
- Department of Radiology and the Research Institute of Radiology, Asan Medical Center, University of Ulsan College of Medicine, Seoul, Korea
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Lee HJ, Kim YJ, Han HY, Seo JY, Hwang CM, Kim K. Ultrasound-guided needle biopsy of large thyroid nodules: Core needle biopsy yields more reliable results than fine needle aspiration. JOURNAL OF CLINICAL ULTRASOUND : JCU 2019; 47:255-260. [PMID: 30820986 DOI: 10.1002/jcu.22721] [Citation(s) in RCA: 9] [Impact Index Per Article: 1.5] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Subscribe] [Scholar Register] [Received: 08/04/2018] [Revised: 01/02/2019] [Accepted: 02/17/2019] [Indexed: 06/09/2023]
Abstract
PURPOSE The objective of this study was to compare the false negative rate, sensitivity and false positive rate of ultrasound (US)-guided fine needle aspiration (FNA) with those of US-guided core needle biopsy (CNB) for large thyroid nodules ≥2.0 cm, which reportedly have an increased risk of thyroid malignancy. METHODS We retrospectively studied surgically confirmed thyroid nodules that had preoperative US-guided FNA or CNB between March 2005 and December 2013. We reviewed nodule size, sonographic features, cytohistologic results, and final surgical pathology. We assessed false negative rates, sensitivity, and false positive rates by biopsy method and nodule size for diagnosis of thyroid malignancy. We assessed complications for procedures. RESULTS US-guided CNB showed better diagnostic performance, in terms of lower false negative rates and greater sensitivity, than US-guided FNA in large thyroid nodules. There was no significant difference in false positive rate according to biopsy methods in large thyroid nodules. The false negative rates of large thyroid nodules (≥2.0 cm) were higher than those of small nodules (<2.0 cm). There were no major complications, and no significant differences in complication according to biopsy methods. CONCLUSION US-guided CNB improved the false negative rate and sensitivity for large nodules. Therefore, US-guided CNB can be considered a useful diagnostic method for large thyroid nodules that might reduce the risk of unnecessary diagnostic surgery.
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Affiliation(s)
- Hyeon Jin Lee
- Department of Radiology, Konyang University Hospital, Konyang University College of Medicine, Daejeon, Republic of Korea
| | - Young Joong Kim
- Department of Radiology, Konyang University Hospital, Konyang University College of Medicine, Daejeon, Republic of Korea
| | - Hye Yeon Han
- Department of Radiology, Daejeon Sun Medical Center, Daejeon, Republic of Korea
| | - Jae Young Seo
- Department of Radiology, Konyang University Hospital, Konyang University College of Medicine, Daejeon, Republic of Korea
| | - Cheol Mog Hwang
- Department of Radiology, Konyang University Hospital, Konyang University College of Medicine, Daejeon, Republic of Korea
| | - KeumWon Kim
- Department of Radiology, Konyang University Hospital, Konyang University College of Medicine, Daejeon, Republic of Korea
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Oh HS, Kwon H, Song E, Jeon MJ, Kim TY, Lee JH, Kim WB, Shong YK, Chung KW, Baek JH, Kim WG. Tumor Volume Doubling Time in Active Surveillance of Papillary Thyroid Carcinoma. Thyroid 2019; 29:642-649. [PMID: 30864894 DOI: 10.1089/thy.2018.0609] [Citation(s) in RCA: 45] [Impact Index Per Article: 7.5] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Indexed: 02/06/2023]
Abstract
Background: Tumor volume (TV) of papillary thyroid carcinoma (PTC) increases exponentially during active surveillance, and the growth rate differs for each patient. TV doubling time (TVDT) is considered a strong dynamic marker for the prediction of the growth rate and progression of the tumor. Methods: This cohort study analyzed 273 PTC patients who underwent active surveillance for more than one year rather than immediate thyroid surgery. TVDT was calculated in each patient, and patients were divided into two groups: rapid-growing (TVDT <5 years) and stable (TVDT ≥5 years). Clinical and initial ultrasonography (US) features between the two groups were compared. Results: The median patient age was 51.1 years (interquartile range [IQR] 42.2-61.0 years), and 76% of the patients were women. The initial TV of PTC was 62.1 mm3 (IQR 28.1-122.8 mm3). During a median of 42 months (IQR 29-61 months) of active surveillance, 10.3% of the patients had a TVDT of less than two years, 5.1% had a TVDT between two and three years, 6.2% had a TVDT between three and four years, 6.6% had a TVDT between four and five years, and 71.8% had a TVDT of five years or more. Patients in the rapid-growing group (77 patients; 28.2%) were significantly younger (p = 0.004) than those in the stable group (196 patients; 71.8%). Being younger than 50 years of age was significantly associated with rapid tumor growth of PTC (odds ratio = 2.31 [confidence interval 1.30-4.31], p = 0.004) in multivariate analysis. In ultrasound findings, macrocalcification was independently associated with rapid tumor growing of PTCs (odds ratio = 4.98 [confidence interval 2.19-11.69], p < 0.001). Conclusions: TVDT is a good indicator for presenting the growing velocity of PTCs during active surveillance. Younger age and macrocalcification in the initial US were associated with rapid-growing PTCs. Determination of TVDT during the early phase of active surveillance may be helpful for the prediction of rapidly progressing PTCs and deciding whether to adopt an early surgical approach.
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Affiliation(s)
- Hye-Seon Oh
- 1 Department of Internal Medicine, Asan Medical Center, University of Ulsan College of Medicine, Seoul, Republic of Korea
- 2 Department of Endocrinology and Metabolism, National Police Hospital, Seoul, Republic of Korea
| | - Hyemi Kwon
- 3 Department of Endocrinology and Metabolism, Kangbuk Samsung Hospital, Sungkyunkwan University School of Medicine, Seoul, Republic of Korea
| | - Eyun Song
- 1 Department of Internal Medicine, Asan Medical Center, University of Ulsan College of Medicine, Seoul, Republic of Korea
| | - Min Ji Jeon
- 1 Department of Internal Medicine, Asan Medical Center, University of Ulsan College of Medicine, Seoul, Republic of Korea
| | - Tae Yong Kim
- 1 Department of Internal Medicine, Asan Medical Center, University of Ulsan College of Medicine, Seoul, Republic of Korea
| | - Jeong Hyun Lee
- 4 Department of Radiology, Asan Medical Center, University of Ulsan College of Medicine, Seoul, Republic of Korea
| | - Won Bae Kim
- 1 Department of Internal Medicine, Asan Medical Center, University of Ulsan College of Medicine, Seoul, Republic of Korea
| | - Young Kee Shong
- 1 Department of Internal Medicine, Asan Medical Center, University of Ulsan College of Medicine, Seoul, Republic of Korea
| | - Ki-Wook Chung
- 5 Department of Surgery, Asan Medical Center, University of Ulsan College of Medicine, Seoul, Republic of Korea
| | - Jung Hwan Baek
- 4 Department of Radiology, Asan Medical Center, University of Ulsan College of Medicine, Seoul, Republic of Korea
| | - Won Gu Kim
- 1 Department of Internal Medicine, Asan Medical Center, University of Ulsan College of Medicine, Seoul, Republic of Korea
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Ha SM, Chung YJ, Ahn HS, Baek JH, Park SB. Echogenic foci in thyroid nodules: diagnostic performance with combination of TIRADS and echogenic foci. BMC Med Imaging 2019; 19:28. [PMID: 30947700 PMCID: PMC6449957 DOI: 10.1186/s12880-019-0328-2] [Citation(s) in RCA: 11] [Impact Index Per Article: 1.8] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/21/2019] [Accepted: 03/26/2019] [Indexed: 02/06/2023] Open
Abstract
BACKGROUND The malignancy risks of various echogenic foci in thyroid nodules are not consistent. The association between malignancy and echogenic foci and various Thyroid Imaging Reporting and Data System (TIRADS) in thyroid nodules has not been evaluated. We evaluated the malignancy probability and diagnostic performance of thyroid nodules with various echogenic foci and in combination with TIRADS. METHODS This retrospective study was approved by Institutional Review Board. The data were retrospectively collected from January 2013 to December 2014. In total, 954 patients (mean age, 50.8 years; range, 13-86 years) with 1112 nodules were included. Using χ2 test, we determined the prevalence of benign and malignant nodules among those with and without echogenic foci; we associated each of 6 echogenic foci types with benign and malignant nodules. Diagnostic performance was compared between the 6 types alone and in combination with various TIRADS. RESULTS Among 1112 nodules, 390 nodules (35.1%) were found to have echogenic foci, and 722 nodules (64.9%) were not. Among nodules with echogenic foci, 254 nodules (65.1%) were malignant. The punctate echogenic foci with comet-tail artifact showed malignancy rate of 77.8% in solid and predominantly solid nodules. Our study demonstrated relatively low PPV (33.3-56.4%) in nodules with large echogenic foci without shadowing, macrocalcification, and peripheral curvilinear or eggshell echogenic foci with or without shadowing. However, when combined with high suspicion category of TIRADS, PPV increased to 50.0-90.9%. CONCLUSION Combination with TIRADS with different types of echogenic foci offer better stratification of the malignancy risk.
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Affiliation(s)
- Su Min Ha
- Department of Radiology, Chung-Ang University Hospital, Chung-Ang University College of Medicine, 102, Heukseok-ro, Dongjak-gu, Seoul, 06973 South Korea
- Department of Radiology, Seoul National College of Medicine, 101 Daehak-ro, Jongno-gu, Seoul, 110-744 Republic of Korea
| | - Yun Jae Chung
- Department of Internal Medicine, Chung-Ang University Hospital, Chung-Ang University College of Medicine, 102, Heukseok-ro, Dongjak-gu, Seoul, 06973 Republic of Korea
| | - Hye Shin Ahn
- Department of Radiology, Chung-Ang University Hospital, Chung-Ang University College of Medicine, 102, Heukseok-ro, Dongjak-gu, Seoul, 06973 South Korea
| | - Jung Hwan Baek
- Department of Radiology and Research Institute of Radiology, University of Ulsan College of Medicine, Asan Medical Center, 86 Asanbyeongwon-Gil, Songpa-gu, Seoul, 05505 South Korea
| | - Sung Bin Park
- Department of Radiology, Chung-Ang University Hospital, Chung-Ang University College of Medicine, 102, Heukseok-ro, Dongjak-gu, Seoul, 06973 South Korea
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Abstract
Thyroid cancers of follicular cell derivation provide excellent phenotype-genotype correlations. Current morphologic classifications are complex and require simplification. Benign adenomas have follicular or papillary architecture and bland cytology. Well-differentiated thyroid carcinomas exhibit follicular architecture, expansile growth, and variable cytologic atypia and invasiveness; low-risk tumors have excellent prognosis after surgical resection whereas widely-invasive and angioinvasive tumors warrant total thyroidectomy and radioablation. Papillary carcinoma is less differentiated; indolent microcarcinomas can be managed by active surveillance, whereas clinical lesions with local or distant spread require therapy. Progression gives rise to poorly differentiated and anaplastic carcinomas that are less common but far more aggressive.
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Affiliation(s)
- Sylvia L Asa
- Department of Laboratory Medicine and Pathobiology, University of Toronto, Elizabeth Street, Toronto, Ontario M5G 2C4, Canada.
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Paja M, del Cura JL, Zabala R, Korta I, Ugalde A, López JI. Core-needle biopsy in thyroid nodules: performance, accuracy, and complications. Eur Radiol 2019; 29:4889-4896. [DOI: 10.1007/s00330-019-06038-6] [Citation(s) in RCA: 18] [Impact Index Per Article: 3.0] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 11/25/2018] [Revised: 12/23/2018] [Accepted: 01/23/2019] [Indexed: 12/14/2022]
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