Diagnostic utility of fine needle aspiration cytology in pediatric thyroid nodules based on Bethesda Classification
-
,
Abstract
Objectives
The Bethesda system for reporting cytopathology (TBSRTC) has been widely adopted in the management of thyroid nodules. Based on the limited pediatric data available, the implied malignancy risk for each of the categories may be significantly different in pediatrics vs. adults, especially in the indeterminate categories (Bethesda Class III or IV). We report the diagnostic utility of fine needle aspiration (FNA) biopsy at our institution based on the Bethesda system and the risk of malignancy in each category.
Methods
We retrospectively reviewed all patients who underwent a thyroid FNA at our tertiary pediatric hospital from 12/1/2002 to 11/30/2018. FNA results were classified according to TBSRTC. Patient demographics, cytology, histopathology, radiological and clinical follow-ups were examined.
Results
A total of 171 patients were included with 203 cytological samples. Average age at initial FNA was 14.7 years (range 6.9–18.6 years). The numbers of nodules reported for Bethesda categories I–VI were 29, 106, 22, 14, 6 and 26, respectively, and the rate of malignancy was: 13.8, 4.7, 22.7, 35.7, 83.3 and 100%, respectively. Use of ultrasound guidance reduced the non-diagnostic rate from 38.1 to 11.5%. Introduction of on-site adequacy testing further reduced the non-diagnostic rate to 6.5% since 2014.
Conclusions
The risk of malignancy for thyroid nodules in this pediatric cohort is higher than reported in adults. However, rates described here are much closer to adult ranges than previously published pediatric cohorts. The addition of adequacy testing improved the non-diagnostic rate of FNA procedures performed with ultrasound guidance.
Research funding: None declared.
Author contributions: Dr. Wen Jiang designed the study and data collection method, collected data with chart reviews, drafted the initial manuscript, reviewed and revised the manuscript, approved the final submission. Dr. Susan Phillips participated in study design, data analysis, reviewed and revised the manuscript. Dr. Robert Newbury provided initial patient identification for the chart reviews, contributed to the cytologic method section of the initial manuscript, reviewed and revised the manuscript. Dr. John Naheedy contributed to the radiologic and procedural section of the initial manuscript, reviewed and revised the manuscript. Dr. Ron Newfield participated in study design, reviewed and revised the manuscript, and approved the final submission. All authors listed assume responsibility and accountability for the results published here.
Competing interests: Authors state no conflict of interest.
References
1. Dinauer, C, Francis, GL. Thyroid cancer in children. Endocrinol Metab Clin North Am 2007;36:779–806. https://doi.org/10.1016/j.ecl.2007.04.002.Search in Google Scholar PubMed
2. Corrias, A, Mussa, F, Baronio, T, Arrigo, M, Salerno, M, Segni, M, et al.. Study Group for Thyroid Diseases of Italian Society for Pediatric Endocrinology and Diabetology (SIEDP/ISPED). Diagnostic features of thyroid nodules in pediatrics. Arch Pediatr Adolesc Med 2010;164:714–9. https://doi.org/10.1001/archpediatrics.2010.114.Search in Google Scholar PubMed
3. Pole, JD, Aleksandra, MZ, Wasserman, JD. Diagnostic and treatment patterns among children, adolescents, and young adults with thyroid cancer in Ontario: 1992-2010. Thyroid 2017;27:1025–33. https://doi.org/10.1089/thy.2016.0629.Search in Google Scholar PubMed
4. Lim, H, Devesa, SS, Sosa, JA, Check, D, Kitahara, CM. Trends in thyroid cancer incidence and mortality in the United States, 1974-2013. J Am Med Assoc 2017;317:1338–48. https://doi.org/10.1001/jama.2017.2719.Search in Google Scholar PubMed PubMed Central
5. Shimura, H, Sobue, T, Takahashi, H, Yasumura, S, Ohira, T, Ohtsuru, A, et al.. Thyroid Examination Unit of the Radiation Medical Center for the Fukushima Health Management Survey Group. Findings of thyroid ultrasound examination within 3 years after the Fukushima nuclear power plant accident: the Fukushima health management survey. J Clin Endocrinol Metab 2018;103:861–9. https://doi.org/10.1210/jc.2017-01603.Search in Google Scholar PubMed
6. Francis, GL, Waguespack, SG, Bauer, AJ, Angelos, P, Benvenga, S, Cerutti, JM, et al.. American Thyroid Association Guidelines Task Force. Management guidelines for children with thyroid nodules and differentiated thyroid cancer. Thyroid 2015;25:716–59. https://doi.org/10.1089/thy.2014.0460.Search in Google Scholar PubMed PubMed Central
7. Cibas, ES, Ali, SZ. NCI Thyroid FNA State of the Science Conference. The Bethesda system for reporting thyroid cytopathology. Am J Clin Pathol 2009;132:658–65. https://doi.org/10.1309/ajcpphlwmi3jv4la.Search in Google Scholar
8. Cibas, ES, Ali, SZ. The 2017 Bethesda system for reporting thyroid cytopathology. Thyroid 2017;27:1341–6. https://doi.org/10.1089/thy.2017.0500.Search in Google Scholar PubMed
9. Cherella, CE, Angell, TE, Richman, DM, Frates, MC, Benson, CB, Moore, FD, et al.. Differences in thyroid nodule cytology and malignancy risk between children and adults. Thyroid 2019;29:1097–104. https://doi.org/10.1089/thy.2018.0728.Search in Google Scholar PubMed PubMed Central
10. Haugen, BR, Alexander, EK, Bible, KC, Doherty, GM, Mandel, SJ, Nikiforov, YE, 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;26:1–133.10.1089/thy.2015.0020Search in Google Scholar PubMed PubMed Central
11. Amirazodi, E, Propst, EJ, Chung, CT, Parra, DA, Wasserman, JD. Pediatric thyroid FNA biopsy: outcomes and impact on management over 24 years at a tertiary care center. Cancer Cytopathol 2016;124:801–10. https://doi.org/10.1002/cncy.21750.Search in Google Scholar PubMed
12. Gupta, A, Ly, S, Castroneves, LA, Frates, MC, Benson, CB, Feldman, HA, et al.. A standardized assessment of thyroid nodules in children confirms higher cancer prevalence than in adults. J Clin Endocrinol Metab 2013;98:3238–45. https://doi.org/10.1210/jc.2013-1796.Search in Google Scholar PubMed PubMed Central
13. Lale, SA, Morgenstern, NN, Chiara, S, Wasserman, P. Fine needle aspiration of thyroid nodules in the pediatric population: a 12-year cyto-histological correlation experience at North Shore-Long Island Jewish Health System. Diagn Cytopathol 2015;43:598–604. https://doi.org/10.1002/dc.23265.Search in Google Scholar PubMed
14. Heider, A, Arnold, S, Jing, X. Bethesda system for reporting thyroid cytopathology in pediatric thyroid nodules. Arch Pathol Lab Med 2020;144:473–7. https://doi.org/10.5858/arpa.2018-0596-oa.Search in Google Scholar PubMed
15. Pinchot, SN, Al-Wagih, H, Schaefer, S, Sippel, R, Chen, H. Accuracy of fine-needle aspiration biopsy for predicting neoplasm or carcinoma in thyroid nodules 4cm or larger. Arch Surg 2009;144:649–55. https://doi.org/10.1001/archsurg.2009.116.Search in Google Scholar PubMed PubMed Central
16. Cipriani, NA, White, MG, Angelos, P, Grogan, RH. Large cytologically benign thyroid nodules do not have high rates of malignancy or false-negative rates and clinical observation should be considered: a meta-analysis. Thyroid 2018;28:1595–608. https://doi.org/10.1089/thy.2018.0221.Search in Google Scholar PubMed
17. Cherella, CE, Feldman, HA, Hollowell, M, Richman, DM, Cibas, ES, Smith, JR, et al.. Natural history and outcomes of cytologically benign thyroid nodules in children. J Clin Endocrinol Metab 2018;103:3557–65. https://doi.org/10.1210/jc.2018-00895.Search in Google Scholar PubMed PubMed Central
18. Bongiovanni, M, Bellevicine, C, Troncone, G, Sykiotis, GP. Approach to cytological indeterminate thyroid nodules. Gland Surg 2019;8(Suppl 2):S98–104. https://doi.org/10.21037/gs.2018.12.06.Search in Google Scholar PubMed PubMed Central
19. Bongiovanni, M, Spitale, A, Faquin, WC, Mazzucchelli, L, Baloch, ZW. The Bethesda system for reporting thyroid cytopathology: a meta-analysis. Acta Cytol 2012;56:333–9. https://doi.org/10.1159/000339959.Search in Google Scholar PubMed
20. Monaco, SE, Pantanowitz, L, Khalbuss, WE, Benkovich, VA, Ozolek, J, Nikiforova, MN, et al.. Cytomorphological and molecular genetic findings in pediatric thyroid fine-needle aspiration. Cancer Cytopathol 2012;120:342–50. https://doi.org/10.1002/cncy.21199.Search in Google Scholar PubMed
21. Nikiforov, YE, Ohori, NP, Hodak, SP, Carty, SE, LeBeau, SO, Ferris, RL, et al.. Impact of mutational testing on the diagnosis and management of patients with cytologically indeterminate thyroid nodules: a prospective analysis of 1056 FNA samples. J Clin Endocrinol Metab 2011;96:3390–97. https://doi.org/10.1210/jc.2011-1469.Search in Google Scholar PubMed PubMed Central
22. Alexander, EK, Kennedy, GC, Baloch, ZW, Cibas, ES, Chudova, D, Diggans, J, et al.. Preoperative diagnosis of benign thyroid nodules with indeterminate cytology. N Engl J Med 2012;367:705–15. https://doi.org/10.1056/nejmoa1203208.Search in Google Scholar PubMed
23. Nikiforov, YE, Carty, SE, Chiosea, SI, Coyne, C, Duvvuri, U, Ferris, RL, et al.. Impact of the multi-gene ThyroSeq next-generation sequencing assay on cancer diagnosis in thyroid nodules with atypia of undetermined significance/follicular lesion of undetermined significance cytology. Thyroid 2015;25:1217–23. https://doi.org/10.1089/thy.2015.0305.Search in Google Scholar PubMed PubMed Central
24. Pastorello, RG, Destefani, C, Pinto, PH, Credidio, CH, Reis, RX, Rodrigues, TA, et al.. The impact of rapid on-site evaluation on thyroid fine-needle aspiration biopsy: a 2-year cancer center institutional experience. Cancer Cytopathol 2018;126:846–52. https://doi.org/10.1002/cncy.22051.Search in Google Scholar PubMed
25. Witt, RL, Sukumar, VR, Gerges, F. Surgeon-performed ultrasound-guided FNAC with on-site cytopathology improves adequacy and accuracy. Laryngoscope 2015;125:1633–6. https://doi.org/10.1002/lary.25214.Search in Google Scholar PubMed
26. Gerhard, R, Boerner, SL. The value of second opinion in thyroid cytology. Cancer Cytopathol 2014;122:611–9. https://doi.org/10.1002/cncy.21436.Search in Google Scholar PubMed
27. Gerhard, R, Boerner, SL. Evaluation of indeterminate thyroid cytology by second-opinion diagnosis or repeat fine-needle aspiration: which is the best approach? Acta Cytol 2015;59:43–50. https://doi.org/10.1159/000369332.Search in Google Scholar PubMed
© 2021 Walter de Gruyter GmbH, Berlin/Boston
Articles in the same Issue
- Frontmatter
- Original Articles
- The utility of next-generation sequencing technologies in diagnosis of Mendelian mitochondrial diseases and reflections on clinical spectrum
- PATRO children, a multi-center, non-interventional study of the safety and effectiveness of Omnitrope® (somatropin) treatment in children: update on the United States cohort
- Effect of vitamin K2 and vitamin D3 on bone mineral density in children with acute lymphoblastic leukemia: a prospective cohort study
- Diagnostic utility of fine needle aspiration cytology in pediatric thyroid nodules based on Bethesda Classification
- Ultrasonographic determination of thyroid volume in infants and children from Aegean region of Turkey and comparison with national and international references
- Association of thyroid autoimmunity and the response to recombinant human growth hormone in Turner syndrome
- Evaluating transition in Turner syndrome in the West of Scotland
- Short-term effects of gonadotropin-releasing hormone analogue treatment on leptin, ghrelin and peptide YY in girls with central precocious puberty
- Metabolic syndrome and risk factors after hematopoietic stem cell transplantation in children and adolescents
- Urinary bisphenol A levels in prepubertal children with exogenous obesity according to presence of metabolic syndrome
- Associations of insulin-induced lipodystrophy in children, adolescents, and young adults with type 1 diabetes mellitus using recombinant human insulin: a cross-sectional study
- Incidence of diabetes in children and adolescents in Dhaka, Bangladesh
- Case Reports
- False-positive very long-chain fatty acids in a case of autoimmune adrenal insufficiency
- Prepubescent unilateral gynecomastia secondary to excessive soy consumption
- Detection of hepatocyte nuclear factor 4A(HNF4A) gene variant as the cause for congenital hyperinsulinism leads to revision of the diagnosis of the mother
- Coexistence of dyschondrosteosis associated to SHOX deficiency, pseudohypoparathyroidism 1B, and chronic autoimmune thyroiditis: a case report
Articles in the same Issue
- Frontmatter
- Original Articles
- The utility of next-generation sequencing technologies in diagnosis of Mendelian mitochondrial diseases and reflections on clinical spectrum
- PATRO children, a multi-center, non-interventional study of the safety and effectiveness of Omnitrope® (somatropin) treatment in children: update on the United States cohort
- Effect of vitamin K2 and vitamin D3 on bone mineral density in children with acute lymphoblastic leukemia: a prospective cohort study
- Diagnostic utility of fine needle aspiration cytology in pediatric thyroid nodules based on Bethesda Classification
- Ultrasonographic determination of thyroid volume in infants and children from Aegean region of Turkey and comparison with national and international references
- Association of thyroid autoimmunity and the response to recombinant human growth hormone in Turner syndrome
- Evaluating transition in Turner syndrome in the West of Scotland
- Short-term effects of gonadotropin-releasing hormone analogue treatment on leptin, ghrelin and peptide YY in girls with central precocious puberty
- Metabolic syndrome and risk factors after hematopoietic stem cell transplantation in children and adolescents
- Urinary bisphenol A levels in prepubertal children with exogenous obesity according to presence of metabolic syndrome
- Associations of insulin-induced lipodystrophy in children, adolescents, and young adults with type 1 diabetes mellitus using recombinant human insulin: a cross-sectional study
- Incidence of diabetes in children and adolescents in Dhaka, Bangladesh
- Case Reports
- False-positive very long-chain fatty acids in a case of autoimmune adrenal insufficiency
- Prepubescent unilateral gynecomastia secondary to excessive soy consumption
- Detection of hepatocyte nuclear factor 4A(HNF4A) gene variant as the cause for congenital hyperinsulinism leads to revision of the diagnosis of the mother
- Coexistence of dyschondrosteosis associated to SHOX deficiency, pseudohypoparathyroidism 1B, and chronic autoimmune thyroiditis: a case report
