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The Bethesda System for Reporting Thyroid Cytopathology (BSRTC)

  • Idris Tolgay OcalEmail author
  • Mohiedean Ghofrani
Chapter

Abstract

Fine needle aspiration (FNA) has been widely accepted as the most accurate and cost-effective method for evaluating thyroid nodules. It is a safe and simple procedure and can be performed by palpation or under image guidance. It has also been established that the sensitivity and specificity of thyroid FNA is greatest for both benign and malignant diagnoses, while in the indeterminate categories, the surgical correlates lack accuracy. To further complicate this issue, there has been a wide range of terminology among cytopathologists for reporting this group of FNAs.

To standardize the terminology for the thyroid FNA reporting and provide better communication among physicians, the National Cancer Institute (NCI) hosted the multidisciplinary “Thyroid Fine Needle Aspiration State of the Science” conference in Bethesda, Maryland, on October 22–23, 2007, with 154 registrants including pathologists, surgeons, endocrinologists, and radiologists. The outcome of this conference was detailed in an atlas in 2010 as the Bethesda System for Reporting Thyroid Cytopathology (BSRTC). A six-tiered reporting system was suggested that included three atypical/indeterminate categories as outlined below:
  • Nondiagnostic or unsatisfactory

  • Benign

  • Atypia of undetermined significance or follicular lesion of undetermined significance (AUS/FLUS)

  • Follicular neoplasm/suspicious for follicular neoplasm (including oncocytic lesions)

  • Suspicious for malignancy

  • Malignant

In this chapter, we summarize the cytopathologic findings and clinical significance of each category in detail, with specific emphasis on the indeterminate category.

Keywords

The Bethesda system Thyroid FNA Indeterminate category 

References

  1. 1.
    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.PubMedPubMedCentralCrossRefGoogle Scholar
  2. 2.
    Cesur M, Corapcioglu D, Bulut S, Gursoy A, Yilmaz AE, Erdogan N, et al. Comparison of palpation-guided fine-needle aspiration biopsy to ultrasound-guided fine-needle aspiration biopsy in the evaluation of thyroid nodules. Thyroid. 2006;16:555–61.PubMedCrossRefGoogle Scholar
  3. 3.
    Danese D, Sciacchitano S, Farsetti A, Andreoli M, Pontecorvi A. Diagnostic accuracy of conventional versus sonography-guided fine-needle aspiration biopsy of thyroid nodules. Thyroid. 1998;8:15–21.PubMedCrossRefGoogle Scholar
  4. 4.
    Deandrea M, Mormile A, Veglio M, Motta M, Pellerito R, Gallone G, et al. Fine-needle aspiration biopsy of the thyroid: comparison between thyroid palpation and ultrasonography. Endocr Pract. 2002;8:282–6.PubMedCrossRefGoogle Scholar
  5. 5.
    Chung YS, Yoo C, Jung JH, Choi HJ, Suh YJ. Review of atypical cytology of thyroid nodule according to the Bethesda system and its beneficial effect in the surgical treatment of papillary carcinoma. J Korean Surg Soc. 2011;81:75–84.PubMedPubMedCentralCrossRefGoogle Scholar
  6. 6.
    Kwak JY, Kim EK, Kim MJ, Hong SW, Choi SH, Son EJ, et al. The role of ultrasound in thyroid nodules with a cytology reading of “suspicious for papillary thyroid carcinoma”. Thyroid. 2008;18:517–22.PubMedCrossRefGoogle Scholar
  7. 7.
    Lee MJ, Hong SW, Chung WY, Kwak JY, Kim MJ, Kim EK. Cytological results of ultrasound-guided fine-needle aspiration cytology for thyroid nodules: emphasis on correlation with sonographic findings. Yonsei Med J. 2011;52:838–44.PubMedPubMedCentralCrossRefGoogle Scholar
  8. 8.
    Jo VY, Renshaw AA, Krane JF. Relative sensitivity of thyroid fine-needle aspiration by tumor type and size. Diagn Cytopathol. 2013;41:871–5.PubMedGoogle Scholar
  9. 9.
    Gharib H, Goellner JR. Fine-needle aspiration biopsy of the thyroid: an appraisal. Ann Intern Med. 1993;118:282–9.PubMedCrossRefGoogle Scholar
  10. 10.
    Amrikachi M, Ramzy I, Rubenfeld S, Wheeler TM. Accuracy of fine-needle aspiration of thyroid. Arch Pathol Lab Med. 2001;125:484–8.PubMedGoogle Scholar
  11. 11.
    Cramer H. Fine-needle aspiration cytology of the thyroid: an appraisal. Cancer. 2000;90:325–9.PubMedCrossRefGoogle Scholar
  12. 12.
    Ravetto C, Colombo L, Dottorini ME. Usefulness of fine-needle aspiration in the diagnosis of thyroid carcinoma: a retrospective study in 37,895 patients. Cancer. 2000;90:357–63.PubMedCrossRefGoogle Scholar
  13. 13.
    Wu HH, Jones JN, Osman J. Fine-needle aspiration cytology of the thyroid: ten years experience in a community teaching hospital. Diagn Cytopathol. 2006;34:93–6.PubMedCrossRefGoogle Scholar
  14. 14.
    Yang J, Schnadig V, Logrono R, Wasserman PG. Fine-needle aspiration of thyroid nodules: a study of 4703 patients with histologic and clinical correlations. Cancer. 2007;111:306–15.PubMedCrossRefGoogle Scholar
  15. 15.
    Yassa L, Cibas ES, Benson CB, Frates MC, Doubilet PM, Gawande AA, et al. Long-term assessment of a multidisciplinary approach to thyroid nodule diagnostic evaluation. Cancer. 2007;111:508–16.PubMedCrossRefGoogle Scholar
  16. 16.
    Ali SZ, Cibas ES, SpringerLink (Online service). The Bethesda system for reporting thyroid cytopathology definitions, criteria and explanatory notes. Boston, MA: Springer Science + Business Media, LLC, 2010:1 online resource.Google Scholar
  17. 17.
    Rabaglia JL, Kabbani W, Wallace L, Holt S, Watumull L, Pruitt J, et al. Effect of the Bethesda system for reporting thyroid cytopathology on thyroidectomy rates and malignancy risk in cytologically indeterminate lesions. Surgery. 2010;148:1267–72; discussion 72–3.PubMedCrossRefGoogle Scholar
  18. 18.
    Crowe A, Linder A, Hameed O, Salih C, Roberson J, Gidley J, et al. The impact of implementation of the Bethesda system for reporting thyroid cytopathology on the quality of reporting, “risk” of malignancy, surgical rate, and rate of frozen sections requested for thyroid lesions. Cancer Cytopathol. 2011;119:315–21.PubMedCrossRefGoogle Scholar
  19. 19.
    Ohori NP, Schoedel KE. Variability in the atypia of undetermined significance/follicular lesion of undetermined significance diagnosis in the Bethesda system for reporting thyroid cytopathology: sources and recommendations. Acta Cytol. 2011;55:492–8.PubMedCrossRefGoogle Scholar
  20. 20.
    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.PubMedCrossRefGoogle Scholar
  21. 21.
    Mehra P, Verma AK. Thyroid cytopathology reporting by the bethesda system: a two-year prospective study in an academic institution. Patholog Res Int. 2015;2015:240505.Google Scholar
  22. 22.
    Singh RS, Wang HH. 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.PubMedCrossRefGoogle Scholar
  23. 23.
    Krane JF, Vanderlaan PA, Faquin WC, Renshaw AA. The atypia of undetermined significance/follicular lesion of undetermined significance:malignant ratio: a proposed performance measure for reporting in the Bethesda system for thyroid cytopathology. Cancer Cytopathol. 2012;120:111–6.PubMedCrossRefGoogle Scholar
  24. 24.
    Ustun H, Astarci HM, Altunkaya C, Yilmaz S, Barin A, Ekici S, et al. Fine-needle aspiration of follicular patterned lesions of the thyroid: diagnosis, management, and follow-up according to thyroid Bethesda system. Acta Cytol. 2012;56:361–9.PubMedCrossRefGoogle Scholar
  25. 25.
    Walts AE, Bose S, Fan X, Frishberg D, Scharre K, de Peralta-Venturina M, et al. A simplified Bethesda system for reporting thyroid cytopathology using only four categories improves intra- and inter-observer diagnostic agreement and provides non-overlapping estimates of malignancy risks. Diagn Cytopathol. 2012;40 Suppl 1:E62–8.PubMedCrossRefGoogle Scholar
  26. 26.
    Baloch ZW, Mandel SJ, LiVolsi VA. Are we ready to modify the Bethesda thyroid fine-needle aspiration classification scheme? Cancer Cytopathol. 2013;121:171–4.PubMedCrossRefGoogle Scholar
  27. 27.
    Onder S, Firat P, Ates D. The Bethesda system for reporting thyroid cytopathology: an institutional experience of the outcome of indeterminate categories. Cytopathology. 2014;25:177–84.PubMedCrossRefGoogle Scholar
  28. 28.
    Ustun B, Chhieng D, Van Dyke A, Carling T, Holt E, Udelsman R, et al. Risk stratification in follicular neoplasm: a cytological assessment using the modified Bethesda classification. Cancer Cytopathol. 2014;122:536–45.PubMedCrossRefGoogle Scholar
  29. 29.
    Broome JT, Solorzano CC. The impact of atypia/follicular lesion of undetermined significance on the rate of malignancy in thyroid fine-needle aspiration: evaluation of the Bethesda system for reporting thyroid cytopathology. Surgery. 2011;150:1234–41.PubMedCrossRefGoogle Scholar
  30. 30.
    Kiernan CM, Broome JT, Solorzano CC. The Bethesda system for reporting thyroid cytopathology: a single-center experience over 5 years. Ann Surg Oncol. 2014;21:3522–7.PubMedPubMedCentralCrossRefGoogle Scholar
  31. 31.
    Park JH, Yoon SO, Son EJ, Kim HM, Nahm JH, Hong S. Incidence and malignancy rates of diagnoses in the bethesda system for reporting thyroid aspiration cytology: an institutional experience. Korean J Pathology. 2014;48:133–9.CrossRefGoogle Scholar
  32. 32.
    Unpublished data on “Intereobserver variability in interpretation of thyroid fine needle aspiration biopsies using the Bethesda system for reporting of thyroid cytology- A focus on atypical cells of undetermined significance/follicular lesion of undetermined significance” from the CAP Cytopathology Committee members; Vijayalakshmi Padmanabhan MBBS, MD, MPH, Carrie Marshall MD, Guliz A Barkan MD, Mohiedean Ghofrani MD, Idris Tolgay Ocal, M.D., Charles Sturgis, Rhona Souers, Daniel F.I. Kurtycz, MD.Google Scholar
  33. 33.
    Goellner JR, Gharib H, Grant CS, Johnson DA. Fine needle aspiration cytology of the thyroid, 1980 to 1986. Acta Cytol. 1987;31:587–90.PubMedGoogle Scholar
  34. 34.
    Choi KU, Kim JY, Park DY, Lee CH, Sol MY, Han KT, et al. Recommendations for the management of cystic thyroid nodules. ANZ J Surg. 2005;75:537–41.PubMedCrossRefGoogle Scholar
  35. 35.
    Deniwar A, Hambleton C, Thethi T, Moroz K, Kandil E. Examining the Bethesda criteria risk stratification of thyroid nodules. Pathol Res Pract. 2015;211:345–8.PubMedCrossRefGoogle Scholar
  36. 36.
    Marchevsky AM, Walts AE, Bose S, Gupta R, Fan X, Frishberg D, et al. Evidence-based evaluation of the risks of malignancy predicted by thyroid fine-needle aspiration biopsies. Diagn Cytopathol. 2010;38:252–9.PubMedGoogle Scholar
  37. 37.
    Theoharis CG, Schofield KM, Hammers L, Udelsman R, Chhieng DC. The Bethesda thyroid fine-needle aspiration classification system: year 1 at an academic institution. Thyroid. 2009;19:1215–23.PubMedCrossRefGoogle Scholar
  38. 38.
    Wu HH, Rose C, Elsheikh TM. The Bethesda system for reporting thyroid cytopathology: an experience of 1,382 cases in a community practice setting with the implication for risk of neoplasm and risk of malignancy. Diagn Cytopathol. 2012;40:399–403.PubMedCrossRefGoogle Scholar
  39. 39.
    Al Maqbali T, Tedla M, Weickert MO, Mehanna H. Malignancy risk analysis in patients with inadequate fine needle aspiration cytology (FNAC) of the thyroid. PLoS One. 2012;7, e49078.PubMedPubMedCentralCrossRefGoogle Scholar
  40. 40.
    Gharib H, Goellner JR, Johnson DA. Fine-needle aspiration cytology of the thyroid. A 12-year experience with 11,000 biopsies. Clin Lab Med. 1993;13:699–709.PubMedGoogle Scholar
  41. 41.
    Anderson TJ, Atalay MK, Grand DJ, Baird GL, Cronan JJ, Beland MD. Management of nodules with initially nondiagnostic results of thyroid fine-needle aspiration: can we avoid repeat biopsy? Radiology. 2014;272:777–84.PubMedCrossRefGoogle Scholar
  42. 42.
    Jo VY, Stelow EB, Dustin SM, Hanley KZ. Malignancy risk for fine-needle aspiration of thyroid lesions according to the Bethesda system for reporting thyroid cytopathology. Am J Clin Pathol. 2010;134:450–6.PubMedCrossRefGoogle Scholar
  43. 43.
    Cerit M, Yucel C, Gocun PU, Poyraz A, Cerit ET, Taneri F. Ultrasound-guided thyroid nodule fine-needle biopsies – comparison of sample adequacy with different sampling techniques, different needle sizes, and with/without onsite cytological analysis. Endokrynol Pol. 2015;66:295–300.PubMedCrossRefGoogle Scholar
  44. 44.
    Ghofrani M, Beckman D, Rimm DL. The value of onsite adequacy assessment of thyroid fine-needle aspirations is a function of operator experience. Cancer. 2006;108:110–3.PubMedCrossRefGoogle Scholar
  45. 45.
    de Meer SG, Schreinemakers JM, Zelissen PM, Stapper G, Sie-Go DM, Rinkes IH, et al. Fine-needle aspiration of thyroid tumors: identifying factors associated with adequacy rate in a large academic center in the Netherlands. Diagn Cytopathol. 2012;40 Suppl 1:E21–6.PubMedCrossRefGoogle Scholar
  46. 46.
    Singh RS, Wang HH. Timing of repeat thyroid fine-needle aspiration in the management of thyroid nodules. Acta Cytol. 2011;55:544–8.PubMedCrossRefGoogle Scholar
  47. 47.
    Lubitz CC, Nagarkatti SS, Faquin WC, Samir AE, Hassan MC, Barbesino G, et al. Diagnostic yield of nondiagnostic thyroid nodules is not altered by timing of repeat biopsy. Thyroid. 2012;22:590–4.PubMedPubMedCentralCrossRefGoogle Scholar
  48. 48.
    Chung J, Youk JH, Kim JA, Kwak JY, Kim EK, Ryu YH, et al. Initially non-diagnostic ultrasound-guided fine needle aspiration cytology of thyroid nodules: value and management. Acta Radiol. 2012;53:168–73.PubMedCrossRefGoogle Scholar
  49. 49.
    Yoon JH, Moon HJ, Kim EK, Kwak JY. Inadequate cytology in thyroid nodules: should we repeat aspiration or follow-up? Ann Surg Oncol. 2011;18:1282–9.PubMedCrossRefGoogle Scholar
  50. 50.
    Haugen B. American Thyroid Association Management Guidelines for adult patients with thyroid nodules and differentiated thyroid cancer. Thyroid. 2015;26(1):1–133.CrossRefGoogle Scholar
  51. 51.
    Baloch ZW, LiVolsi VA, Asa SL, Rosai J, Merino MJ, Randolph G, et al. Diagnostic terminology and morphologic criteria for cytologic diagnosis of thyroid lesions: a synopsis of the National Cancer Institute Thyroid Fine-Needle Aspiration State of the Science Conference. Diagn Cytopathol. 2008;36:425–37.PubMedCrossRefGoogle Scholar
  52. 52.
    Rosai J, Carcangiu ML, DeLellis RA, American Registry of Pathology, Universities Associated for Research and Education in Pathology, Center for Medical Education Technologies (Rockville Md.). Tumors of the thyroid gland. Atlas of tumor pathology Third series,. Washington, D.C.: Published by the Armed Forces Institute of Pathology, under the auspices of Universities Associated for Research and Education in Pathology,, 1994:1 computer laser optical disc.Google Scholar
  53. 53.
    Bongiovanni M, Krane JF, Cibas ES, Faquin WC. The atypical thyroid fine-needle aspiration: past, present, and future. Cancer Cytopathol. 2012;120:73–86.PubMedCrossRefGoogle Scholar
  54. 54.
    Chen JC, Pace SC, Khiyami A, McHenry CR. Should atypia of undetermined significance be subclassified to better estimate risk of thyroid cancer? Am J Surg. 2014;207:331–6; discussion 5–6.PubMedCrossRefGoogle Scholar
  55. 55.
    Ho AS, Sarti EE, Jain KS, Wang H, Nixon IJ, Shaha AR, et al. Malignancy rate in thyroid nodules classified as Bethesda category III (AUS/FLUS). Thyroid. 2014;24:832–9.PubMedPubMedCentralCrossRefGoogle Scholar
  56. 56.
    Horne MJ, Chhieng DC, Theoharis C, Schofield K, Kowalski D, Prasad ML, et al. Thyroid follicular lesion of undetermined significance: evaluation of the risk of malignancy using the two-tier sub-classification. Diagn Cytopathol. 2012;40:410–5.PubMedCrossRefGoogle Scholar
  57. 57.
    Hyeon J, Ahn S, Shin JH, Oh YL. The prediction of malignant risk in the category “atypia of undetermined significance/follicular lesion of undetermined significance” of the Bethesda system for reporting thyroid cytopathology using subcategorization and BRAF mutation results. Cancer Cytopathol. 2014;122:368–76.PubMedCrossRefGoogle Scholar
  58. 58.
    Olson MT, Clark DP, Erozan YS, Ali SZ. Spectrum of risk of malignancy in subcategories of ‘atypia of undetermined significance’. Acta Cytol. 2011;55:518–25.PubMedCrossRefGoogle Scholar
  59. 59.
    Park HJ, Moon JH, Yom CK, Kim KH, Choi JY, Choi SI, et al. Thyroid “atypia of undetermined significance” with nuclear atypia has high rates of malignancy and BRAF mutation. Cancer Cytopathol. 2014;122:512–20.PubMedCrossRefGoogle Scholar
  60. 60.
    Renshaw AA. Does a repeated benign aspirate change the risk of malignancy after an initial atypical thyroid fine-needle aspiration? Am J Clin Pathol. 2010;134:788–92.PubMedCrossRefGoogle Scholar
  61. 61.
    Wu HH, Inman A, Cramer HM. Subclassification of “atypia of undetermined significance” in thyroid fine-needle aspirates. Diagn Cytopathol. 2014;42:23–9.PubMedCrossRefGoogle Scholar
  62. 62.
    Gocun PU, Karakus E, Bulutay P, Akturk M, Akin M, Poyraz A. What is the malignancy risk for atypia of undetermined significance? three years’ experience at a university hospital in Turkey. Cancer Cytopathol. 2014;122:604–10.PubMedCrossRefGoogle Scholar
  63. 63.
    Iskandar ME, Bonomo G, Avadhani V, Persky M, Lucido D, Wang B, et al. Evidence for overestimation of the prevalence of malignancy in indeterminate thyroid nodules classified as Bethesda category III. Surgery. 2015;157:510–7.PubMedCrossRefGoogle Scholar
  64. 64.
    Wong LQ, LiVolsi VA, Baloch ZW. Diagnosis of atypia/follicular lesion of undetermined significance: an institutional experience. Cytojournal. 2014;11:23.PubMedPubMedCentralCrossRefGoogle Scholar
  65. 65.
    Faquin WC, Baloch ZW. Fine-needle aspiration of follicular patterned lesions of the thyroid: diagnosis, management, and follow-up according to National Cancer Institute (NCI) recommendations. Diagn Cytopathol. 2010;38:731–9.PubMedGoogle Scholar
  66. 66.
    Baloch Z, LiVolsi VA, Jain P, Jain R, Aljada I, Mandel S, et al. Role of repeat fine-needle aspiration biopsy (FNAB) in the management of thyroid nodules. Diagn Cytopathol. 2003;29:203–6.PubMedCrossRefGoogle Scholar
  67. 67.
    Nikiforov YE, Seethala RR, Tallini G, et al. Nomenclature revision for encapsulated follicular variant of papillary thyroid carcinoma: a paradigm shift to reduce overtreatment of indolent tumors. JAMA Oncol. 2016.Google Scholar
  68. 68.
    Maletta F, Massa F, Torregrossa L, et al. Cytological features of “non-invasive follicular thyroid neoplasm with papillary-like nuclear features” and their correlation with tumor histology. Hum Pathol. 2016.Google Scholar
  69. 69.
    Ocal IT, Ghofrani M. Follicular neoplasias of thyroid, fine-needle aspiration cytology. Pathology Case Reviews. 2015;20:115–20.CrossRefGoogle Scholar
  70. 70.
    Deshpande V, Kapila K, Sai KS, Verma K. Follicular neoplasms of the thyroid. Decision tree approach using morphologic and morphometric parameters. Acta Cytol. 1997;41:369–76.PubMedCrossRefGoogle Scholar
  71. 71.
    Lubitz CC, Faquin WC, Yang J, Mekel M, Gaz RD, Parangi S, et al. Clinical and cytological features predictive of malignancy in thyroid follicular neoplasms. Thyroid. 2010;20:25–31.PubMedCrossRefGoogle Scholar
  72. 72.
    Baloch ZW, Fleisher S, LiVolsi VA, Gupta PK. Diagnosis of “follicular neoplasm”: a gray zone in thyroid fine-needle aspiration cytology. Diagn Cytopathol. 2002;26:41–4.PubMedCrossRefGoogle Scholar
  73. 73.
    Goldstein RE, Netterville JL, Burkey B, Johnson JE. Implications of follicular neoplasms, atypia, and lesions suspicious for malignancy diagnosed by fine-needle aspiration of thyroid nodules. Ann Surg. 2002;235:656–62; discussion 62–4.PubMedPubMedCentralCrossRefGoogle Scholar
  74. 74.
    Lee SH, Baek JS, Lee JY, Lim JA, Cho SY, Lee TH, et al. Predictive factors of malignancy in thyroid nodules with a cytological diagnosis of follicular neoplasm. Endocr Pathol. 2013;24:177–83.PubMedCrossRefGoogle Scholar
  75. 75.
    Williams BA, Bullock MJ, Trites JR, Taylor SM, Hart RD. Rates of thyroid malignancy by FNA diagnostic category. J Otolaryngology – Head & Neck Surgery = Le Journal d’oto-rhino-laryngologie et de chirurgie cervico-faciale. 2013;42:61.Google Scholar
  76. 76.
    Baloch ZW, Gupta PK, Yu GH, Sack MJ, LiVolsi VA. Follicular variant of papillary carcinoma. Cytologic and histologic correlation. Am J Clin Pathol. 1999;111:216–22.PubMedCrossRefGoogle Scholar
  77. 77.
    Manimaran D, Karthikeyan TM, Khan DM, Raman RT. Follicular variant of papillary thyroid carcinoma: cytological indicators of diagnostic value. J Clinical and Diagnostic Research JCDR. 2014;8:46–8.Google Scholar
  78. 78.
    Logani S, Gupta PK, LiVolsi VA, Mandel S, Baloch ZW. Thyroid nodules with FNA cytology suspicious for follicular variant of papillary thyroid carcinoma: follow-up and management. Diagn Cytopathol. 2000;23:380–5.PubMedCrossRefGoogle Scholar
  79. 79.
    Powari M, Dey P, Saikia UN. Fine needle aspiration cytology of follicular variant of papillary carcinoma of thyroid. Cytopathology. 2003;14:212–5.PubMedCrossRefGoogle Scholar
  80. 80.
    Shih SR, Shun CT, Su DH, Hsiao YL, Chang TC. Follicular variant of papillary thyroid carcinoma: diagnostic limitations of fine needle aspiration cytology. Acta Cytol. 2005;49:383–6.PubMedCrossRefGoogle Scholar
  81. 81.
    Ustun B, Chhieng D, Prasad ML, Holt E, Hammers L, Carling T, et al. Follicular Variant of Papillary Thyroid Carcinoma: Accuracy of FNA Diagnosis and Implications for Patient Management. Endocr Pathol. 2014;25(3):257–64.PubMedCrossRefGoogle Scholar
  82. 82.
    Pu RT, Yang J, Wasserman PG, Bhuiya T, Griffith KA, Michael CW. Does Hurthle cell lesion/neoplasm predict malignancy more than follicular lesion/neoplasm on thyroid fine-needle aspiration? Diagn Cytopathol. 2006;34:330–4.PubMedCrossRefGoogle Scholar
  83. 83.
    Deveci MS, Deveci G, LiVolsi VA, Baloch ZW. Fine-needle aspiration of follicular lesions of the thyroid. Diagnosis and follow-Up Cytojournal. 2006;3:9.PubMedCrossRefGoogle Scholar
  84. 84.
    Nesland JM, Sobrinho-Simoes MA, Holm R, Sambade MC, Johannessen JV. Hurthle-cell lesions of the thyroid: a combined study using transmission electron microscopy, scanning electron microscopy, and immunocytochemistry. Ultrastruct Pathol. 1985;8:269–90.PubMedCrossRefGoogle Scholar
  85. 85.
    Kini SR, Miller JM, Hamburger JI, Smith MJ. Cytopathologic features of medullary carcinoma of the thyroid. Arch Pathol Lab Med. 1984;108:156–9.PubMedGoogle Scholar
  86. 86.
    Renshaw AA. Hurthle cell carcinoma is a better gold standard than Hurthle cell neoplasm for fine-needle aspiration of the thyroid: defining more consistent and specific cytologic criteria. Cancer. 2002;96:261–6.PubMedCrossRefGoogle Scholar
  87. 87.
    Carson HJ, Castelli MJ, Gattuso P. Incidence of neoplasia in Hashimoto’s thyroiditis: a fine-needle aspiration study. Diagn Cytopathol. 1996;14:38–42.PubMedCrossRefGoogle Scholar
  88. 88.
    Cersosimo E, Gharib H, Suman VJ, Goellner JR. “Suspicious” thyroid cytologic findings: outcome in patients without immediate surgical treatment. Mayo Clin Proc. 1993;68:343–8.PubMedCrossRefGoogle Scholar
  89. 89.
    Leiker AJ, Yen TW, Cheung K, Evans DB, Wang TS. Cost analysis of thyroid lobectomy and intraoperative frozen section versus total thyroidectomy in patients with a cytologic diagnosis of “suspicious for papillary thyroid cancer”. Surgery. 2013;154:1307–13; discussion 13–4.PubMedCrossRefGoogle Scholar
  90. 90.
    DeLellis RA. Pathology and genetics of tumours of endocrine organs. Lyon: IARC Press; 2004.Google Scholar
  91. 91.
    Fulciniti F, Benincasa G, Vetrani A, Palombini L. Follicular variant of papillary carcinoma: cytologic findings on FNAB samples-experience with 16 cases. Diagn Cytopathol. 2001;25:86–93.PubMedCrossRefGoogle Scholar
  92. 92.
    Fadda G, Fiorino MC, Mule A, LiVolsi VA. Macrofollicular encapsulated variant of papillary thyroid carcinoma as a potential pitfall in histologic and cytologic diagnosis. A report of three cases. Acta Cytol. 2002;46:555–9.PubMedCrossRefGoogle Scholar
  93. 93.
    Goellner JR, Johnson DA. Cytology of cystic papillary carcinoma of the thyroid. Acta Cytol. 1982;26:797–808.PubMedGoogle Scholar
  94. 94.
    Moreira AL, Waisman J, Cangiarella JF. Aspiration cytology of the oncocytic variant of papillary adenocarcinoma of the thyroid gland. Acta Cytol. 2004;48:137–41.PubMedCrossRefGoogle Scholar
  95. 95.
    Baloch ZW, LiVolsi VA. Warthin-like papillary carcinoma of the thyroid. Arch Pathol Lab Med. 2000;124:1192–5.PubMedGoogle Scholar
  96. 96.
    Ghossein R, Livolsi VA. Papillary thyroid carcinoma tall cell variant. Thyroid. 2008;18:1179–81.PubMedCrossRefGoogle Scholar
  97. 97.
    Jayaram G. Cytology of columnar-cell variant of papillary thyroid carcinoma. Diagn Cytopathol. 2000;22:227–9.PubMedCrossRefGoogle Scholar
  98. 98.
    Mesonero CE, Jugle JE, Wilbur DC, Nayar R. Fine-needle aspiration of the macrofollicular and microfollicular subtypes of the follicular variant of papillary carcinoma of the thyroid. Cancer. 1998;84:235–44.PubMedCrossRefGoogle Scholar
  99. 99.
    Ghofrani M, Ocal IT. Medullary thyroid carcinoma: a brief review of pathogenesis, diagnosis, and treatment. Pathology Case Reviews. 2015;20:204–9.CrossRefGoogle Scholar
  100. 100.
    Pusztaszeri MP, Bongiovanni M, Faquin WC. Update on the cytologic and molecular features of medullary thyroid carcinoma. Adv Anat Pathol. 2014;21:26–35.PubMedCrossRefGoogle Scholar
  101. 101.
    Akbulut S, Sogutcu N. A high level of carcinoembryonic antigen as initial manifestation of medullary thyroid carcinoma in a patient with subclinical hyperthyroidism. Int Surg. 2011;96:254–9.PubMedCrossRefGoogle Scholar
  102. 102.
    Filie AC, Asa SL, Geisinger KR, Logani S, Merino M, Nikiforov YE, et al. Utilization of ancillary studies in thyroid fine needle aspirates: a synopsis of the National Cancer Institute Thyroid Fine Needle Aspiration State of the Science Conference. Diagn Cytopathol. 2008;36:438–41.PubMedCrossRefGoogle Scholar
  103. 103.
    Carcangiu ML, Zampi G, Rosai J. Poorly differentiated (“insular”) thyroid carcinoma. A reinterpretation of Langhans’ “wuchernde Struma”. Am J Surg Pathol. 1984;8:655–68.PubMedCrossRefGoogle Scholar
  104. 104.
    Ghofrani M, Sosa JA, Ocal IT, Angeletti C. Fine needle aspiration of poorly differentiated oxyphilic (Hurthle cell) thyroid carcinoma: a case report. Acta Cytol. 2006;50:560–2.PubMedCrossRefGoogle Scholar
  105. 105.
    Miettinen M, Franssila KO. Variable expression of keratins and nearly uniform lack of thyroid transcription factor 1 in thyroid anaplastic carcinoma. Hum Pathol. 2000;31:1139–45.PubMedCrossRefGoogle Scholar
  106. 106.
    Bolfi F, Domingues MA, Sobrinho-Simoes M, Soares P, Celestino R, Castilho EC, et al. Primary squamous cell carcinoma of the thyroid diagnosed as anaplastic carcinoma: failure in fine-needle aspiration cytology?. Case Rep Pathol. 2014;2014:301780.Google Scholar
  107. 107.
    Pedersen RK, Pedersen NT. Primary non-Hodgkin’s lymphoma of the thyroid gland: a population based study. Histopathology. 1996;28:25–32.PubMedCrossRefGoogle Scholar
  108. 108.
    Lerma E, Arguelles R, Rigla M, Otal C, Cubero JM, Bague S, et al. Comparative findings of lymphocytic thyroiditis and thyroid lymphoma. Acta Cytol. 2003;47:575–80.PubMedCrossRefGoogle Scholar
  109. 109.
    Boonyaarunnate T, Olson MT, Ali SZ. Impact of flow cytometry in thyroid cytopathology. Acta Cytol. 2013;57:562–6.PubMedCrossRefGoogle Scholar
  110. 110.
    Chung AY, Tran TB, Brumund KT, Weisman RA, Bouvet M. Metastases to the thyroid: a review of the literature from the last decade. Thyroid. 2012;22:258–68.PubMedCrossRefGoogle Scholar
  111. 111.
    Nakhjavani M, Gharib H, Goellner JR, Heerden JA. Direct extension of malignant lesions to the thyroid gland from adjacent organs: report of 17 cases. Endocr Pract. 1999;5:69–71.PubMedCrossRefGoogle Scholar
  112. 112.
    HooKim K, Gaitor J, Lin O, Reid MD. Secondary tumors involving the thyroid gland: a multi-institutional analysis of 28 cases diagnosed on fine-needle aspiration. Diagn Cytopathol. 2015;43:904–11.PubMedCrossRefGoogle Scholar
  113. 113.
    Nakhjavani MK, Gharib H, Goellner JR, van Heerden JA. Metastasis to the thyroid gland. A report of 43 cases. Cancer. 1997;79:574–8.PubMedCrossRefGoogle Scholar
  114. 114.
    Chiumento C, Fiorentino A, Castaldo G, Fusco V. A case of thyroid metastasis of nasopharyngeal cancer. Tumori. 2011;97:24e-6e.PubMedGoogle Scholar
  115. 115.
    Lam KY, Lo CY. Metastatic tumors of the thyroid gland: a study of 79 cases in Chinese patients. Arch Pathol Lab Med. 1998;122:37–41.PubMedGoogle Scholar
  116. 116.
    Darouassi Y, Touati MM, Chihani M, Nadour K, Boussouga M, Ammar H, et al. Chondrosarcoma metastasis in the thyroid gland: a case report. J Med Case Rep. 2014;8:157.PubMedPubMedCentralCrossRefGoogle Scholar
  117. 117.
    Heffess CS, Wenig BM, Thompson LD. Metastatic renal cell carcinoma to the thyroid gland: a clinicopathologic study of 36 cases. Cancer. 2002;95:1869–78.PubMedCrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2017

Authors and Affiliations

  1. 1.Pathology and Laboratory Medicine, Division of Anatomic Pathology, Department of Laboratory Medicine/PathologyMayo Clinic ArizonaScottsdaleUSA
  2. 2.Cytopathology, PeaceHealth LaboratoriesVancouverUSA

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