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The 2023 Bethesda system for reporting thyroid cytopathology: novi sub sole, subdivision is no more debatable, in thyroidology

The 2010 Bethesda system for reporting thyroid cytopathology (TBSRTC) was initially proposed at the National Cancer Institute (NCI) Thyroid Fine Needle Aspiration (FNA) State of the Art and Science Conference held in Bethesda, Maryland, 2007. Afterward, the 2010 TBSRTC, first edition, suggested thyroidologists to utilize a standardized, six-category-based reporting system for thyroid FNA in the States and worldwide by Cibas and Ali, founders of this lexicon, which was published in the 19th volume of Thyroid11 Cibas ES, Ali SZ. The Bethesda system for reporting thyroid cytopathology. Thyroid. 2009;19(11):1159-65. https://doi.org/10.1089/thy.2009.0274
https://doi.org/10.1089/thy.2009.0274...
. Wielding TBSRTC has also been endorsed by the 2015 American Thyroid Association (ATA) management guidelines22 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):1-133. https://doi.org/10.1089/thy.2015.0020
https://doi.org/10.1089/thy.2015.0020...
similar to the 2009 ATA guidelines33 Cooper DS, Doherty GM, Haugen BR, Kloos RT, Lee SL, Mandel SJ, et al. Revised American thyroid association management guidelines for patients with thyroid nodules and differentiated thyroid cancer. Thyroid. 2009;19(11):1167-214. https://doi.org/10.1089/thy.2009.0110
https://doi.org/10.1089/thy.2009.0110...
, which was the revision of the 2006 ATA guidelines44 Cooper DS, Doherty GM, Haugen BR, Kloos RT, Lee SL, Mandel SJ, et al. Management guidelines for patients with thyroid nodules and differentiated thyroid cancer. Thyroid. 2006;16(2):109-42. https://doi.org/10.1089/thy.2006.16.109
https://doi.org/10.1089/thy.2006.16.109...
, through the management of this delicate endocrine gland11 Cibas ES, Ali SZ. The Bethesda system for reporting thyroid cytopathology. Thyroid. 2009;19(11):1159-65. https://doi.org/10.1089/thy.2009.0274
https://doi.org/10.1089/thy.2009.0274...
99 Sengul D, Sengul I. Reassessing combining real-time elastography with fine-needle aspiration biopsy to identify malignant thyroid nodules. Am J Med Case Rep. 2021;9(11):552-3. https://doi.org/10.12691/ajmcr-9-11-9
https://doi.org/10.12691/ajmcr-9-11-9...
.

On May 28–June 01, 2016, a special 2½ h symposium entitled “The Bethesda System for reporting thyroid cytopathology: past, present, future” was moderated by Ali and Vielh at the 19th International Congress of Cytology, ICC, in Pacifico Yokohama, Japan1010 Ali SZ, Vielh P, Pusztaszeri M, Rossi D, Faquin WC, Bishop JA, et al. The Bethesda system for reporting thyroid cytopathology: past, present, future at the 19th International Congress of Cytology in Pacifico Yokohama, Japan, on 28 May–01 June 2016, Symposium 12, Yokohama; 2016.,1111 Ali SZ, Cibas ES. The Bethesda system for reporting thyroid cytopathology II. Acta Cytol. 2016;60(5):397-8. https://doi.org/10.1159/000451071
https://doi.org/10.1159/000451071...
. In addition to this, Pusztaszeri et al.1212 Pusztaszeri M, Rossi ED, Auger M, Baloch Z, Bishop J, Bongiovanni M, et al. The Bethesda system for reporting thyroid cytopathology: proposed modifications and updates for the second edition from an international panel. Acta Cytol. 2016;60(5):399-405. https://doi.org/10.1159/000451020
https://doi.org/10.1159/000451020...
and Ali et al.1010 Ali SZ, Vielh P, Pusztaszeri M, Rossi D, Faquin WC, Bishop JA, et al. The Bethesda system for reporting thyroid cytopathology: past, present, future at the 19th International Congress of Cytology in Pacifico Yokohama, Japan, on 28 May–01 June 2016, Symposium 12, Yokohama; 2016.,1111 Ali SZ, Cibas ES. The Bethesda system for reporting thyroid cytopathology II. Acta Cytol. 2016;60(5):397-8. https://doi.org/10.1159/000451071
https://doi.org/10.1159/000451071...
also discussed briefly the consensus of the aforementioned panel, recommendations, proposed modifications, and updates for a second edition of TBSRTC by anticipating its emerging date in early 2018. However, the 2017 TBSRTC, second edition, was then published in the 27th volume of Thyroid, by rectifying the implied risk of malignancy (ROM) for each category, remarkable for indeterminate cytology, molecular testing recommendations interpolating explanatory notes in order to state some may represent the newly established noninvasive follicular thyroid neoplasm with papillary-like nuclear features, NIFTP1313 Cibas ES, Ali SZ. The 2017 Bethesda system for reporting thyroid cytopathology. Thyroid. 2017;27(11):1341-6. https://doi.org/10.1089/thy.2017.0500
https://doi.org/10.1089/thy.2017.0500...
.

Mater artium necessitas. After these two successful former editions worldwide, a third edition of this lexicon, the 2023 TBSRTC, has been announced currently again by Ali et al.1414 Ali SZ, Baloch ZW, Cochand-Priollet B, Schmitt FC, Vielh P, VanderLaan PA. The 2023 Bethesda system for reporting thyroid cytopathology. Thyroid. 2023;33(9):1039-44. https://doi.org/10.1089/thy.2023.0141
https://doi.org/10.1089/thy.2023.0141...
. Of note, the up-to-date third edition has been published and available online on July 08, 2023 in Thyroid in order to shed light on (a) simplifying the six diagnostic categories with a single name for each, adopting the new histologic terminologies according to the 2022 World Health Organization (WHO) Classification of Thyroid Neoplasms: (i) nondiagnostic; (ii) benign, (iii) atypia of undetermined significance (AUS), (iv) follicular neoplasm, (v) suspicious for malignancy, and (vi) malignant; (b) updating and refining each category by implying ROM based on data reported after the second edition; (c) suggesting an average ROM for each category, besides an expected range of risk of carcinoma; (d) subdividing AUS into two subgroups based on the implied ROM and molecular profiling tests; (e) insertion and discussion of pediatric thyroid diseases and ROMs with the management of algorithms; (f) appending two new chapters of expanded use of molecular and ancillary testing in thyroid cytopathology, and clinical perspectives and imaging findings1414 Ali SZ, Baloch ZW, Cochand-Priollet B, Schmitt FC, Vielh P, VanderLaan PA. The 2023 Bethesda system for reporting thyroid cytopathology. Thyroid. 2023;33(9):1039-44. https://doi.org/10.1089/thy.2023.0141
https://doi.org/10.1089/thy.2023.0141...
.

Herewith, we sincerely appreciate one of the masters of thyroid cytopathology in order to illuminate the challenging issue, noted for this crucial subdivision, in their updated1414 Ali SZ, Baloch ZW, Cochand-Priollet B, Schmitt FC, Vielh P, VanderLaan PA. The 2023 Bethesda system for reporting thyroid cytopathology. Thyroid. 2023;33(9):1039-44. https://doi.org/10.1089/thy.2023.0141
https://doi.org/10.1089/thy.2023.0141...
lexicon. To date, assessment for indeterminate cytology, particularly category III, has still been one of the most challenging issues in thyroidology1515 Sengul I, Sengul D. Comment on: ‘evaluating treatment options in managing thyroid nodules with indeterminate cytology of TBSRTC in thyroidology: addendum aut non?’ Rev Assoc Med Bras (1992). 2022;68(7):973-4. https://doi.org/10.1590/1806-9282.20220383
https://doi.org/10.1590/1806-9282.202203...
2020 Sengul D, Sengul I. Are there any variation in neutrophil lymphocyte ratio, mean platelet volume, and platelet count between papillary thyroid cancer and benign nodular thyroid diseases? Sanamed. 2018;13(1):11-6. https://doi.org/10.24125/sanamed.v13i1.209
https://doi.org/10.24125/sanamed.v13i1.2...
. To this end, in February 2021, we emphasized whether or not it is essential to maintain category III as a unique and indivisible category among indeterminate cytology in the 67th volume of Rev Assoc Med Bras2121 Sengul I, Sengul D. Focusing on thyroid nodules in suspense: 10-15 mm with repeat cytology, category III, the Bethesda system for reporting thyroid cytopathology, TBSRTC. Rev Assoc Med Bras (1992). 2021;67(2):166-7. https://doi.org/10.1590/1806-9282.67.02.20200828
https://doi.org/10.1590/1806-9282.67.02....
. Afterward, we published an article in the same volume of Rev Assoc Med Bras, about blurred lines for managing thyroid nodules in the era of category III in a possible forthcoming TBSRTC, 3rd edition on October 2021. Of note, we postulated in this publication in the 67th volume of Rev Assoc Med Bras that the so-called subdivision demand and so kind of reality in category III, TBSRTC, 2nd edition as (i) Category IIIA: AUS/FLUS without nuclear atypia (AUS/FLUS wo NA) and (ii) Category IIIB: AUS/FLUS with nuclear atypia (AUS/FLUS w NA)2222 Sengul I, Sengul D. Blurred lines for management of thyroid nodules in the era of atypia of undetermined significance/ follicular lesion of undetermined significance: novel subdivisions of categories IIIA and IIIB in a possible forthcoming the Bethesda system for reporting thyroid cytopathology, 3rd edition; amending versus unnecessary? Rev Assoc Med Bras (1992). 2021;67(10):1385-6. https://doi.org/10.1590/1806-9282.20210763
https://doi.org/10.1590/1806-9282.202107...
, which is very similar to that of Ali et al.1414 Ali SZ, Baloch ZW, Cochand-Priollet B, Schmitt FC, Vielh P, VanderLaan PA. The 2023 Bethesda system for reporting thyroid cytopathology. Thyroid. 2023;33(9):1039-44. https://doi.org/10.1089/thy.2023.0141
https://doi.org/10.1089/thy.2023.0141...
. Finally, we have also currently recommended working with subdivisions instead of insisting on a monolithic category III to be able to resolve the issue of the ongoing debate on indeterminate cytology in our epub ahead of the print article in Ultrasonography with a submission date of June 08, 20232323 Sengul D, Sengul I. Subdivision of intermediate suspicion, the 2021 K-TIRADS, and category III, indeterminate cytology, the 2017 TBSRTC, 2nd edition, in thyroidology: let bygones be bygones? Ultrasonography. 2023;42(4):600-1. https://doi.org/10.14366/usg.23113
https://doi.org/10.14366/usg.23113...
.

Breviter, we have emphasized opting for a subdivision for AUS (formerly AUS/FLUS) and the value of NA in our three works before the updated third edition. NAs have non-negligible clues in these nodules. E fructu arbor cognoscitur. Bene diagnoscitur bene curatur. We are deeply grateful to Cibas and Ali, founders and doyennes of this crucial thyroid lexicon invaluably stating “just keep study” instead of “just keep stu(ea)dy” for AUS of TBSRTC, which will be accepted worldwide.

  • Funding: none.

ACKNOWLEDGMENTS

We thank all the study participants.

REFERENCES

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    Cibas ES, Ali SZ. The Bethesda system for reporting thyroid cytopathology. Thyroid. 2009;19(11):1159-65. https://doi.org/10.1089/thy.2009.0274
    » https://doi.org/10.1089/thy.2009.0274
  • 2
    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):1-133. https://doi.org/10.1089/thy.2015.0020
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  • 3
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    » https://doi.org/10.1089/thy.2009.0110
  • 4
    Cooper DS, Doherty GM, Haugen BR, Kloos RT, Lee SL, Mandel SJ, et al. Management guidelines for patients with thyroid nodules and differentiated thyroid cancer. Thyroid. 2006;16(2):109-42. https://doi.org/10.1089/thy.2006.16.109
    » https://doi.org/10.1089/thy.2006.16.109
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    Sengul D, Sengul I. Reassessing combining real-time elastography with fine-needle aspiration biopsy to identify malignant thyroid nodules. Am J Med Case Rep. 2021;9(11):552-3. https://doi.org/10.12691/ajmcr-9-11-9
    » https://doi.org/10.12691/ajmcr-9-11-9
  • 10
    Ali SZ, Vielh P, Pusztaszeri M, Rossi D, Faquin WC, Bishop JA, et al. The Bethesda system for reporting thyroid cytopathology: past, present, future at the 19th International Congress of Cytology in Pacifico Yokohama, Japan, on 28 May–01 June 2016, Symposium 12, Yokohama; 2016.
  • 11
    Ali SZ, Cibas ES. The Bethesda system for reporting thyroid cytopathology II. Acta Cytol. 2016;60(5):397-8. https://doi.org/10.1159/000451071
    » https://doi.org/10.1159/000451071
  • 12
    Pusztaszeri M, Rossi ED, Auger M, Baloch Z, Bishop J, Bongiovanni M, et al. The Bethesda system for reporting thyroid cytopathology: proposed modifications and updates for the second edition from an international panel. Acta Cytol. 2016;60(5):399-405. https://doi.org/10.1159/000451020
    » https://doi.org/10.1159/000451020
  • 13
    Cibas ES, Ali SZ. The 2017 Bethesda system for reporting thyroid cytopathology. Thyroid. 2017;27(11):1341-6. https://doi.org/10.1089/thy.2017.0500
    » https://doi.org/10.1089/thy.2017.0500
  • 14
    Ali SZ, Baloch ZW, Cochand-Priollet B, Schmitt FC, Vielh P, VanderLaan PA. The 2023 Bethesda system for reporting thyroid cytopathology. Thyroid. 2023;33(9):1039-44. https://doi.org/10.1089/thy.2023.0141
    » https://doi.org/10.1089/thy.2023.0141
  • 15
    Sengul I, Sengul D. Comment on: ‘evaluating treatment options in managing thyroid nodules with indeterminate cytology of TBSRTC in thyroidology: addendum aut non?’ Rev Assoc Med Bras (1992). 2022;68(7):973-4. https://doi.org/10.1590/1806-9282.20220383
    » https://doi.org/10.1590/1806-9282.20220383
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    Sengul D, Sengul I. Minimum minimorum: thyroid minimally invasive FNA, less is more concept? Volens nolens? Rev Assoc Med Bras (1992). 2022;68(3):275-6. https://doi.org/10.1590/1806-9282.20211181
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    Sengul I, Sengul D. Emphasis on the novel age cutoff, 55 years, for postsurgical adjuvant radioiodine as consideration for American thyroid association ¾ low-intermediate risk differentiated thyroid carcinoma. Rev Assoc Med Bras (1992). 2021;67(4):485-6. https://doi.org/10.1590/1806-9282.20201013
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    Sengul I, Sengul D. Notes on ‘elastography for the diagnosis of high-suspicion thyroid nodules based on the 2015 American thyroid association guidelines: a multicenter study’. North Clin Istanb. 2020;8(1):109-10. https://doi.org/10.14744/nci.2020.74240
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    Sengul D, Sengul I. Is there any link between a kind of thyrocyte dysfunction, hypothyroidism, and inflammatory hematologic parameters in the cases having the benign thyroid nodules?: a 5-year single-centre experience. Sanamed. 2018;13(1):35-40. https://doi.org/10.24125/sanamed.v13i1.211
    » https://doi.org/10.24125/sanamed.v13i1.211
  • 20
    Sengul D, Sengul I. Are there any variation in neutrophil lymphocyte ratio, mean platelet volume, and platelet count between papillary thyroid cancer and benign nodular thyroid diseases? Sanamed. 2018;13(1):11-6. https://doi.org/10.24125/sanamed.v13i1.209
    » https://doi.org/10.24125/sanamed.v13i1.209
  • 21
    Sengul I, Sengul D. Focusing on thyroid nodules in suspense: 10-15 mm with repeat cytology, category III, the Bethesda system for reporting thyroid cytopathology, TBSRTC. Rev Assoc Med Bras (1992). 2021;67(2):166-7. https://doi.org/10.1590/1806-9282.67.02.20200828
    » https://doi.org/10.1590/1806-9282.67.02.20200828
  • 22
    Sengul I, Sengul D. Blurred lines for management of thyroid nodules in the era of atypia of undetermined significance/ follicular lesion of undetermined significance: novel subdivisions of categories IIIA and IIIB in a possible forthcoming the Bethesda system for reporting thyroid cytopathology, 3rd edition; amending versus unnecessary? Rev Assoc Med Bras (1992). 2021;67(10):1385-6. https://doi.org/10.1590/1806-9282.20210763
    » https://doi.org/10.1590/1806-9282.20210763
  • 23
    Sengul D, Sengul I. Subdivision of intermediate suspicion, the 2021 K-TIRADS, and category III, indeterminate cytology, the 2017 TBSRTC, 2nd edition, in thyroidology: let bygones be bygones? Ultrasonography. 2023;42(4):600-1. https://doi.org/10.14366/usg.23113
    » https://doi.org/10.14366/usg.23113

Publication Dates

  • Publication in this collection
    13 Nov 2023
  • Date of issue
    2023

History

  • Received
    23 Aug 2023
  • Accepted
    26 Aug 2023
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