Skip to main content

Advertisement

SpringerLink
Log in

The Implementation of the Bethesda System for Reporting Thyroid Cytopathology Improves Malignancy Detection Despite Lower Rate of Thyroidectomy in Indeterminate Nodules

  • Original Scientific Report
  • Published:
World Journal of Surgery Aims and scope Submit manuscript

Abstract

Background

The Bethesda system for reporting thyroid cytopathology (TBSRTC) was developed in 2009 to standardize the terminology for interpreting fine-needle aspiration (FNA) specimens.

Methods

A historical prospective case series design was employed. The study group included patients with a thyroid nodule classified as TBSRTC AUS/FLUS (B3) or FN/SFN (B4) in 2011–2012 in a tertiary university-affiliated medical center. Rates of surgery and malignancy detection were compared to our pre-TBSRTC (1999–2000) study.

Results

Of 3927 nodules aspirated, 575 (14.6 %) were categorized as B3/B4. Complete data were available for 322. Thyroidectomy was performed in 123 (38.2 %) cases: 66/250 (26.4 %) B3 and 57/72 (79.2 %) B4. Differentiated thyroid cancer was found in 66 (53.7 %) patients: 30/66 (45.5 %) B3 and 36/57 (63.2 %) B4 (p = 0.075). Operated patients were younger than the non-operated (B3: 52.4 ± 16 vs. 59.7 ± 13 years, p = 0.009; B4: 51.7 ± 15 vs. 60.5 ± 14 years, p = 0.042), and operated B3 nodules were larger than the non-operated (27.2 vs. 22.2 mm, p = 0.014). Additional FNA was done in 160 patients (49.7 %): 137/250 (54.8 %) B3 and 23/72 (31.9 %) B4 (p = 0.002). The additional B3 nodules aspirations yielded a diagnosis of B2 in 84 patients (61.3 %), B3 in 48 (35 %), and B4 in 5 (3.6 %). Of the 23 repeated B4 aspirations, B2 was reported in 5 (21.7 %), B3 in 12 (52.2 %), B4 in 4 (17.4 %), and B6 in 2 (8.7 %). The number of aspirated nodules was twice that reported in 1999–2000. The rate of indeterminate nodules increased from 6 to 14.6 %, the surgery rate decreased from 52.3 to 38.2 %, and the accuracy of malignancy diagnosis increased from 25.9 to 53.7 %.

Conclusions

The application of TBSRTC significantly improves diagnostic accuracy for indeterminate thyroid nodules, leading to higher rates of malignancy detection despite lower rates of thyroidectomies.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig.1

Similar content being viewed by others

References

  1. Wiest PW, Hartshorne MF, Inskip PD et al (1998) Thyroid palpation versus high-resolution thyroid ultrasonography in the detection of nodules. J Ultrasound Med 17:487–496

    CAS  PubMed  Google Scholar 

  2. Cronan JJ (1998) Thyroid nodules: is it time to turn off the US machines? Radiology 247:602–604

    Article  Google Scholar 

  3. Mortensen JD, Woolner LB, Bennett WA (1955) Gross and microscopic findings in clinically normal thyroid glands. J Clin Endocrinol Metab 15:1270–1280

    Article  CAS  PubMed  Google Scholar 

  4. Caruso DR, Mazzaferri EL (1991) Fine needle aspiration biopsy in the management of thyroid nodules. Endocrinologist 1:194–202

    Article  Google Scholar 

  5. Hegedus L (2004) Clinical practice. The thyroid nodule. N Engl J Med 351:1764–1771

    Article  PubMed  Google Scholar 

  6. Redman R, Yoder BJ, Massol NA (2001) Perceptions of diagnostic terminology and cytopathologic reporting of fine needle aspiration biopsies of thyroid nodules: a survey of clinicians and pathologists. Thyroid 16:1003–1008

    Article  Google Scholar 

  7. Cibas ES, Syed AZ (2009) NCI thyroid FNA state of the science conference. The Bethesda system for reporting thyroid cytopathology. Am J Clin Pathol 132:658–665

    Article  PubMed  Google Scholar 

  8. Cooper DS, Doherty GM, Haugen BR et al (2006) Management guidelines for patients with thyroid nodules and differentiated thyroid cancer. Thyroid 16:109–142

    Article  PubMed  Google Scholar 

  9. Cooper DS, Doherty GM, Haugen BR et al (2009) Revised American Thyroid Association management guidelines for patients with thyroid nodules and differentiated thyroid cancer. Thyroid 19:1167–1214

    Article  PubMed  Google Scholar 

  10. Chen JC, Pace SC, Chen BA et al (2012) Yield of repeat fine-needle aspiration biopsy and rate of malignancy in patients with atypia or follicular lesion of undetermined significance: the impact of the Bethesda system for reporting thyroid cytopathology. Surgery 152:1037–1044

    Article  PubMed  Google Scholar 

  11. McElroy MK, Mahooti S, Hasten F (2014) A single institution experience with the new bethesda system for reporting thyroid cytopathology: correlation with existing cytologic, clinical, and histological data. Diagn Cytopathol 42(7):564–569

    Article  PubMed  Google Scholar 

  12. Crowe A, Linder A, Hameed O et al (2011) 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 119:315–321

    Article  PubMed  Google Scholar 

  13. Sullivan PS, Hirschowitz SL, Fung PC et al (2014) The impact of atypia/follicular lesion of undetermined significance and repeat fine-needle aspiration: 5 years before and after implementation of the Bethesda system. Cancer Cytopathol 122(12):866–872. doi:10.1002/cncy.21468 [Epub ahead of print]

    Article  PubMed  Google Scholar 

  14. Rabaglia JL, Kabbani W, Wallace L et al (2010) Effect of the Bethesda system for reporting thyroid cytopathology on thyroidectomy rates and malignancy risk in cytologically indeterminate lesions. Surgery 148:1267–1272

    Article  PubMed  Google Scholar 

  15. Boonyaarunnate T, Olson MT, Ali SZ (2013) ‘Suspicious for a follicular neoplasm’ before and after the Bethesda system for reporting thyroid cytopathology: impact of standardized terminology. Acta Cytol 57:455–456

    Article  PubMed  Google Scholar 

  16. Broome JT, Solorzano CC (2011) 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 150:1234–1241

    Article  PubMed  Google Scholar 

  17. Harvey AM, Mody DR, Amrikachi M (2013) Thyroid fine-needle aspiration reporting rates and outcomes before and after Bethesda implementation within a combined academic and community hospital system. Arch Pathol Lab Med 137:1664–1668

    Article  PubMed  Google Scholar 

  18. Bahar G, Braslavsky D, Shpitzer T, Feinmesser R, Avidan S, Popovtzer A, Karl S (2003) The cytological and clinical value of the thyroid “follicular lesion”. Am J Otolaryngol 24:217–220

    Article  PubMed  Google Scholar 

  19. Sosa JA, Hanna JW, Robinson KA et al (2013) Increases in thyroid nodule fine-needle aspirations, operations, and diagnoses of thyroid cancer in the United States. Surgery 154:1420–1426

    Article  PubMed  Google Scholar 

  20. Layfield LJ, Morton MJ, Cramer HM et al (2009) Implications of the proposed thyroid fine-needle aspiration category of “follicular lesion of undetermined significance”: a five-year multi-institutional analysis. Diagn Cytopathol 37:710–714

    Article  PubMed  Google Scholar 

  21. Bongiovanni M, Spitale A, Faquin WC et al (2012) The Bethesda system for reporting thyroid cytopathology: a meta-analysis. Acta Cytol 56:333–339

    Article  PubMed  Google Scholar 

  22. Jo VY, Stelow EB, Dustin SM et al (2010) Malignancy risk for fine-needle aspiration of thyroid lesions according to the Bethesda system for reporting thyroid cytopathology. Am J Clin Pathol 134:450–456

    Article  PubMed  Google Scholar 

  23. Renshaw AA (2010) Should ‘atypical follicular cells’ in thyroid fine-needle aspirates be subclassified? Cancer Cytopathol 118:186–189

    Article  PubMed  Google Scholar 

  24. Nayar R, Ivanovic M (2009) The indeterminate thyroid fine-needle aspiration: experience from an academic center using terminology similar to that proposed in the 2007 National Cancer Institute Thyroid Fine Needle Aspiration State of the Science Conference. Cancer Cytopathol 117:195–202

    Article  Google Scholar 

  25. Theoharis CG, Schofield KM, Hammers L et al (2009) The Bethesda thyroid fine-needle aspiration classification system: year 1 at an academic institution. Thyroid 19:1215–1223

    Article  PubMed  Google Scholar 

  26. Kim SK, Hwang TS, Yoo YB et al (2011) Surgical results of thyroid nodules according to a management guideline based on the BRAF(V600E) mutation status. J Clin Endocrinol Metabol 96:658–664

    Article  CAS  Google Scholar 

  27. Her-Juing WuH, Rose C, Elsheikh TM (2012) The Bethesda system for reporting thyroid cytopathology: an experience of 1382 cases in a community practice setting with the implication for risk of neoplasm and risk of malignancy. Diagn Cytopathol 40:399–403

    Article  Google Scholar 

  28. Bongiovanni M, Crippa S, Baloch Z et al (2012) Comparison of 5-tiered and 6-tiered diagnostic systems for the reporting of thyroid cytopathology: a multi-institutional study. Cancer Cytopathol 120:117–125

    Article  PubMed  Google Scholar 

  29. Bohacek L, Milas M, Mitchell J et al (2012) Diagnostic accuracy of surgery on performed ultrasound-guided fine-needle aspiration of thyroid nodules. Ann Surg Oncol 19:45–51

    Article  PubMed  Google Scholar 

  30. Ho AS, Sarti EE, Jain KS et al (2014) Malignancy rate in thyroid nodules classified as Bethesda category III (AUS/FLUS). Thyroid 24:832–839

    Article  PubMed  Google Scholar 

  31. VanderLaan PA, Marqusee E, Krane JF (2011) Clinical outcome for atypia of undetermined significance in thyroid fine-needle aspirations: should repeated FNA be the preferred initial approach? Am J Clin Pathol 135:770

    Article  PubMed  Google Scholar 

  32. Vanderlaan PA, Krane JF, Cibas ES (2011) The frequency of ‘atypia of undetermined significance’ interpretations for thyroid fine-needle aspirations is negatively correlated with histologically proven malignant outcomes. Acta Cytol 55:512–517

    Article  PubMed  Google Scholar 

  33. Stelow EB, Bardales RH, Crary GS et al (2005) Interobserver variability in thyroid fine-needle aspiration interpretation of lesions showing predominantly colloid and follicular groups. Am J Clin Pathol 124:239–244

    Article  PubMed  Google Scholar 

  34. Wang CC, Friedman L, Kennedy GC et al (2011) A large multicenter correlation study of thyroid nodule cytopathology and histopathology. Thyroid 21:243–251

    Article  PubMed Central  PubMed  Google Scholar 

  35. Nikiforov YE, Ohori NP, Hodak SP et al (2011) 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 96:3390–3397

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  36. Alexander EK, Kennedy GC, Baloch ZW et al (2012) Preoperative diagnosis of benign thyroid nodules with indeterminate cytology. N Engl J Med 367:705–715

    Article  CAS  PubMed  Google Scholar 

  37. McIver B (2013) Evaluation of the thyroid nodule. Oral Oncol 49:645–653

    Article  PubMed  Google Scholar 

  38. Bernet V, Hupart KH et al (2014) AACE/ACE Disease State Commentary: molecular diagnostic testing of thyroid nodules with indeterminate cytopathology. Endocr Pract 20:360–363

    Article  PubMed  Google Scholar 

Download references

Conflicting interests

No conflicting interests exist.

Financial disclosure

No competing financial interests exist.

Author information

Author notes

    Authors and Affiliations

    1. Endocrine Institute, Rabin Medical Center, 49100, Petach Tikva, Israel

      Dania Hirsch, Eyal Robenshtok & Carlos Benbassat

    2. Department of Otorhinolaryngology and Head and Neck Surgery, Rabin Medical Center, 49100, Petach Tikva, Israel

      Gideon Bachar

    3. Institute of Pathology, Rabin Medical Center, 49100, Petach Tikva, Israel

      Diana Braslavsky

    4. Sackler Faculty of Medicine, Tel Aviv University, Tel Aviv, Israel

      Dania Hirsch, Eyal Robenshtok, Gideon Bachar, Diana Braslavsky & Carlos Benbassat

    Authors
    1. Dania Hirsch
      View author publications

      You can also search for this author in PubMed Google Scholar

    2. Eyal Robenshtok
      View author publications

      You can also search for this author in PubMed Google Scholar

    3. Gideon Bachar
      View author publications

      You can also search for this author in PubMed Google Scholar

    4. Diana Braslavsky
      View author publications

      You can also search for this author in PubMed Google Scholar

    5. Carlos Benbassat
      View author publications

      You can also search for this author in PubMed Google Scholar

    Corresponding author

    Correspondence to Dania Hirsch.

    Additional information

    Hirsch D. and Robenshtok E. contributed equally to this work.

    Rights and permissions

    Reprints and permissions

    About this article

    Check for updates. Verify currency and authenticity via CrossMark

    Cite this article

    Hirsch, D., Robenshtok, E., Bachar, G. et al. The Implementation of the Bethesda System for Reporting Thyroid Cytopathology Improves Malignancy Detection Despite Lower Rate of Thyroidectomy in Indeterminate Nodules. World J Surg 39, 1959–1965 (2015). https://doi.org/10.1007/s00268-015-3032-6

    Download citation

    • Published:

    • Issue Date:

    • DOI: https://doi.org/10.1007/s00268-015-3032-6

    Keywords

    Search

    Navigation