Are Bethesda III Thyroid Nodules More Aggressive than Bethesda IV Thyroid Nodules When Found to Be Malignant?
Abstract
Simple Summary
Abstract
1. Introduction
2. Materials and Methods
2.1. Patient Selection
2.2. Statistical Analysis
3. Results
4. Discussion
5. Conclusions
Author Contributions
Funding
Conflicts of Interest
References
- Davies, L.; Welch, H.G. Current thyroid cancer trends in the United States. JAMA Otolaryngol. Head Neck Surg. 2014, 140, 317–322. [Google Scholar] [CrossRef]
- Tan, G.H.; Gharib, H. Thyroid incidentalomas: Management approaches to nonpalpable nodules discovered incidentally on thyroid imaging. Ann. Intern. Med. 1997, 126, 226–231. [Google Scholar] [CrossRef] [PubMed]
- Dean, D.S.; Gharib, H. Epidemiology of thyroid nodules. Best Pract. Res. Clin. Endocrinol. Metab. 2008, 22, 901–911. [Google Scholar] [CrossRef] [PubMed]
- Haugen, B.R.; Alexander, E.K.; Bible, K.C.; Doherty, G.M.; Mandel, S.J.; Nikiforov, Y.E.; Pacini, F.; Randolph, G.W.; Sawka, A.M.; Schlumberger, M.; et al. 2015 American Thyroid Association Management Guidelines for Adult Patients with Thyroid Nodules and Differentiated Thyroid Cancer: The American Thyroid Association Guidelines Task Force on Thyroid Nodules and Differentiated Thyroid Cancer. Thyroid 2016, 26, 1–133. [Google Scholar] [CrossRef] [PubMed]
- Yang, J.; Schnadig, V.; Logrono, R.; Wasserman, P.G. Fine-needle aspiration of thyroid nodules: A study of 4703 patients with histologic and clinical correlations. Cancer 2007, 111, 306–315. [Google Scholar] [CrossRef] [PubMed]
- Cibas, E.S.; Ali, S.Z. The Bethesda System for Reporting Thyroid Cytopathology. Thyroid 2009, 19, 1159–1165. [Google Scholar] [CrossRef]
- Cibas, E.S.; Ali, S.Z. The 2017 Bethesda System for Reporting Thyroid Cytopathology. Thyroid 2017, 27, 1341–1346. [Google Scholar] [CrossRef]
- Iskandar, M.E.; Bonomo, G.; Avadhani, V.; Persky, M.; Lucido, D.; Wang, B.; Marti, J.L. Evidence for overestimation of the prevalence of malignancy in indeterminate thyroid nodules classified as Bethesda category III. Surgery 2015, 157, 510–517. [Google Scholar] [CrossRef]
- VanderLaan, P.A.; Marqusee, E.; Krane, J.F. Usefulness of diagnostic qualifiers for thyroid fine-needle aspirations with atypia of undetermined significance. Am. J. Clin. Pathol. 2011, 136, 572–577. [Google Scholar] [CrossRef]
- Renshaw, A.A. Subclassification of atypical cells of undetermined significance in direct smears of fine-needle aspirations of the thyroid: Distinct patterns and associated risk of malignancy. Cancer Cytopathol. 2011, 119, 322–327. [Google Scholar] [CrossRef]
- Wu, H.H.; Inman, A.; Cramer, H.M. Subclassification of “atypia of undetermined significance” in thyroid fine-needle aspirates. Diagn Cytopathol. 2014, 42, 23–29. [Google Scholar] [CrossRef] [PubMed]
- Singh, R.S.; Wang, H.H. Eliminating the “atypia of undetermined significance/follicular lesion of undetermined significance” category from the Bethesda system for reporting thyroid cytopathology. Am. J. Clin. Pathol. 2011, 136, 896–902. [Google Scholar] [CrossRef] [PubMed]
- Horne, M.J.; Chhieng, D.C.; Theoharis, C.; Schofield, K.; Kowalski, D.; Prasad, M.L.; Hammers, L.; Udelsman, R.; Adeniran, A.J. Thyroid follicular lesion of undetermined significance: Evaluation of the risk of malignancy using the two-tier sub-classification. Diagn. Cytopathol. 2012, 40, 410–415. [Google Scholar] [CrossRef]
- Olson, M.T.; Clark, D.P.; Erozan, Y.S.; Ali, S.Z. Spectrum of risk of malignancy in subcategories of “atypia of undetermined significance”. Acta Cytol. 2011, 55, 518–525. [Google Scholar] [CrossRef] [PubMed]
- Ohashi, R.; Kawahara, K.; Namimatsu, S.; Igarashi, T.; Sakatani, T.; Sugitani, I.; Naito, Z. Clinicopathological significance of a solid component in papillary thyroid carcinoma. Histopathology 2017, 70, 775–781. [Google Scholar] [CrossRef]
- Yaprak Bayrak, B.; Eruyar, A.T. Malignancy rates for Bethesda III and IV thyroid nodules: A retrospective study of the correlation between fine-needle aspiration cytology and histopathology. BMC Endocr. Disord. 2020, 20, 48. [Google Scholar] [CrossRef]
- Al-Kurd, A.; Maree, A.; Mizrahi, I.; Kaganov, K.; Weinberger, J.M.; Mali, B.; Mazeh, H.; Hirshoren, N. An Institutional Analysis of Malignancy Rate in Bethesda III and IV Nodules of the Thyroid. Am. J. Otolaryngol. Head Neck Surg. 2019, 2, 1034. [Google Scholar]
- Ho, A.S.; Sarti, E.E.; Jain, K.S.; Wang, H.; Nixon, I.J.; Shaha, A.R.; Shah, J.P.; Kraus, D.H.; Ghossein, R.; Fish, S.A.; et al. Malignancy rate in thyroid nodules classified as Bethesda category III (AUS/FLUS). Thyroid 2014, 24, 832–839. [Google Scholar] [CrossRef]
- Kleiman, D.A.; Beninato, T.; Soni, A.; Shou, Y.; Zarnegar, R.; Fahey, T.J., 3rd. Does Bethesda category predict aggressive features in malignant thyroid nodules? Ann. Surg. Oncol. 2013, 20, 3484–3490. [Google Scholar] [CrossRef]
- Park, V.Y.; Kim, E.K.; Kwak, J.Y.; Yoon, J.H.; Moon, H.J. Associations between Bethesda categories and tumor characteristics of conventional papillary thyroid carcinoma. Ultrasonography 2018, 37, 323–329. [Google Scholar] [CrossRef]
- VanderLaan, P.A.; Marqusee, E.; Krane, J.F. Features associated with locoregional spread of papillary carcinoma correlate with diagnostic category in the Bethesda System for reporting thyroid cytopathology. Cancer Cytopathol. 2012, 120, 245–253. [Google Scholar] [CrossRef] [PubMed]
- Liu, X.; Medici, M.; Kwong, N.; Angell, T.E.; Marqusee, E.; Kim, M.I.; Larsen, P.R.; Cho, N.L.; Nehs, M.A.; Ruan, D.T.; et al. Bethesda Categorization of Thyroid Nodule Cytology and Prediction of Thyroid Cancer Type and Prognosis. Thyroid 2016, 26, 256–261. [Google Scholar] [CrossRef] [PubMed]
- Lloyd, R.V.; Osamura, R.Y.; Klöppel, G.; Rosai, J. (Eds.) WHO Classification of Tumours of Endocrine Organs, 4th ed.; IARC: Lyon, France, 2017. [Google Scholar]
- Ohashi, R. Solid variant of papillary thyroid carcinoma: An under-recognized entity. Endocr. J. 2020, 67, 241–248. [Google Scholar] [CrossRef] [PubMed]
- Giorgadze, T.A.; Scognamiglio, T.; Yang, G.C. Fine-needle aspiration cytology of the solid variant of papillary thyroid carcinoma: A study of 13 cases with clinical, histologic, and ultrasound correlations. Cancer Cytopathol. 2015, 123, 71–81. [Google Scholar] [CrossRef] [PubMed]
- Park, J.S.; Chang, J.W.; Liu, L.; Jung, S.N.; Koo, B.S. Clinical implications of microscopic extrathyroidal extension in patients with papillary thyroid carcinoma. Oral Oncol. 2017, 72, 183–187. [Google Scholar] [CrossRef]
- Shaha, A.R. Extrathyroidal extension-what does it mean. Oral Oncol. 2017, 68, 50–52. [Google Scholar] [CrossRef]
- Krasner, J.R.; Alyouha, N.; Pusztaszeri, M.; Forest, V.I.; Hier, M.P.; Avior, G.; Payne, R.J. Molecular mutations as a possible factor for determining extent of thyroid surgery. J. Otolaryngol. Head Neck Surg. 2019, 48, 51. [Google Scholar] [CrossRef]
- Macerola, E.; Rago, T.; Proietti, A.; Basolo, F.; Vitti, P. The mutational analysis in the diagnostic work-up of thyroid nodules: The real impact in a center with large experience in thyroid cytopathology. J. Endocrinol. Investig. 2019, 42, 157–166. [Google Scholar] [CrossRef]
- Ferrari, S.M.; Fallahi, P.; Ruffilli, I.; Elia, G.; Ragusa, F.; Paparo, S.R.; Ulisse, S.; Baldini, E.; Giannini, R.; Miccoli, P.; et al. Molecular testing in the diagnosis of differentiated thyroid carcinomas. Gland Surg. 2018, 7 (Suppl. 1), S19–S29. [Google Scholar] [CrossRef]
- Penna, G.C.; Vaisman, F.; Vaisman, M.; Sobrinho-Simões, M.; Soares, P. Molecular Markers Involved in Tumorigenesis of Thyroid Carcinoma: Focus on Aggressive Histotypes. Cytogenet. Genome Res. 2016, 150, 194–207. [Google Scholar] [CrossRef]
Population | Bethesda III (%) N = 367 | Bethesda IV (%) N = 261 |
---|---|---|
Mean Age | ||
• 15–30 • 31–50 • 51–70 • 71+ | 21 (5.7) 121 (33.0) 186 (50.7) 39 (10.6) | 21 (8.0) 94 (36.0) 118 (45.2) 28 (10.7) |
Gender | ||
• Male • Female | 69 (18.8) 298 (81.2) | 42 (16.1) 219 (83.9) |
Nodule Size | ||
• <1 cm • 1–2 cm • 2–3 cm • 3 cm+ | 17 (4.6) 117 (32.0) 88 (24.0) 144 (39.3) | 5 (1.9) 92 (35.2) 62 (23.8) 102 (39.1) |
Pathology | ||
• Benign • Malignant | 168 (45.8) 199 (54.2) | 45 (17.2) 216 (82.8) |
Aggressive Features | ||
• Not Present • Present | 330 (89.9) 37 (10.1) | 239 (91.6) 22 (8.4) |
Aggressive Features | Bethesda III 199 Malignant | Bethesda IV 216 Malignant | p Value |
---|---|---|---|
Tall cell variant of PTC | 6 (3.0) | 4 (1.9) | 0.34 |
Solid variant of PTC | 7 (3.5) | 1 (0.5) | 0.013 |
Columnar cell variant of PTC | 0 (0) | 1 (0.5) | 0.36 |
Diffusing sclerosing variant of PTC | 0 (0) | 0 (0) | - |
Hobnail variant of PTC | 3 (1.5) | 1 (0.5) | 0.21 |
Poorly differentiated thyroid carcinoma | 2 (1.0) | 4 (1.0) | 0.59 |
ETE | 2 (1.0) | 1 (0.5) | 0.43 |
LN+ | 17 (8.5) | 10 (4.6) | 0.036 |
Features | No Molecular | Molecular | p Value |
---|---|---|---|
Malignant | |||
| 94 (47.2) 83 (38.4) | 105 (52.7) 133 (61.5) | 0.001 0.092 |
Aggressive features | |||
| 12 (32.4) 4 (18.2) | 25 (67.6) 18 (81.8) | 0.011 0.004 |
© 2020 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
Turkdogan, S.; Pusztaszeri, M.; Forest, V.-I.; Hier, M.P.; Payne, R.J. Are Bethesda III Thyroid Nodules More Aggressive than Bethesda IV Thyroid Nodules When Found to Be Malignant? Cancers 2020, 12, 2563. https://doi.org/10.3390/cancers12092563
Turkdogan S, Pusztaszeri M, Forest V-I, Hier MP, Payne RJ. Are Bethesda III Thyroid Nodules More Aggressive than Bethesda IV Thyroid Nodules When Found to Be Malignant? Cancers. 2020; 12(9):2563. https://doi.org/10.3390/cancers12092563
Chicago/Turabian StyleTurkdogan, Sena, Marc Pusztaszeri, Veronique-Isabelle Forest, Michael P. Hier, and Richard J. Payne. 2020. "Are Bethesda III Thyroid Nodules More Aggressive than Bethesda IV Thyroid Nodules When Found to Be Malignant?" Cancers 12, no. 9: 2563. https://doi.org/10.3390/cancers12092563
APA StyleTurkdogan, S., Pusztaszeri, M., Forest, V.-I., Hier, M. P., & Payne, R. J. (2020). Are Bethesda III Thyroid Nodules More Aggressive than Bethesda IV Thyroid Nodules When Found to Be Malignant? Cancers, 12(9), 2563. https://doi.org/10.3390/cancers12092563