Skip to main content

Advertisement

SpringerLink
Log in

Clinical practice guidelines on ultrasound-guided fine needle aspiration biopsy of thyroid nodules: a critical appraisal using AGREE II

  • Original Article
  • Published:
Endocrine Aims and scope Submit manuscript

Abstract

Purpose

To appraise the quality of current guidelines on fine needle aspiration biopsy (FNAB) of thyroid nodules for adults using the AGREE II quality assessment tool.

Methods

We conducted an online search for guidelines on FNAB of thyroid nodules published between 2013 and October 2018. They were evaluated by four independent reviewers previously trained to apply the AGREE II instrument, which is organized into items and domains. A fifth independent reviewer calculated scores for each domain and guideline as well as inter-appraiser agreement.

Results

Six sets of guidelines were included, respectively, provided by the American Thyroid Association (ATA), the American Association of Clinical Endocrinologists/American College of Endocrinology/Associazione Medici Endocrinologi (AACE/ACE/AME), the Korean Society of Thyroid Radiology (KSThR), the European Thyroid Association (ETA), the American College of Radiology (ACR) and the Korean Society of Radiology and National Evidence-Based Healthcare Collaborating Agency (KSR/NECA). Five out of the six guidelines (ATA, AACE/ACE/AME, ETA, ACR and KSR/NECA) reached a high level of overall quality, having at least five domain scores >60%. An average level of overall quality was achieved in one case (KSThR recommendations). Inter-appraiser agreement ranged from moderate to excellent.

Conclusions

Overall, the quality of guidelines on FNAB of thyroid nodules is satisfactory when evaluated using the AGREE II instrument.

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

Similar content being viewed by others

References

  1. S. Guth, U. Theune, J. Aberle, A. Galach, C.M. Bamberger, Very high prevalence of thyroid nodules detected by high frequency (13 MHz) ultrasound examination. Eur. J. Clin. Invest. 39(8), 699–706 (2009). https://doi.org/10.1111/j.1365-2362.2009.02162.x

    Article  CAS  PubMed  Google Scholar 

  2. C.F. Dietrich, T. Muller, J. Bojunga, Y. Dong, G. Mauri, M. Radzina, M. Dighe, X.W. Cui, F. Grunwald, A. Schuler, A. Ignee, H. Korkusuz, Statement and Recommendations on Interventional Ultrasound as a Thyroid Diagnostic and Treatment Procedure. Ultrasound Med. Biol. 44(1), 14–36 (2018). https://doi.org/10.1016/j.ultrasmedbio.2017.08.1889

    Article  PubMed  Google Scholar 

  3. G. Mauri, C.M. Pacella, E. Papini, L.M. Sconfienza, L. Solbiati, Proceedings of the first Italian conference on thyroid minimally invasive treatments and foundation of the Italian research group for thyroid minimally invasive procedures. Int. J. Hyperth. 34(5), 603–605 (2018). https://doi.org/10.1080/02656736.2018.1442590

  4. E.A. Mittendorf, S.W. Tamarkin, C.R. McHenry, The results of ultrasound-guided fine-needle aspiration biopsy for evaluation of nodular thyroid disease. Surgery 132(4), 648–653 (2002). discussion 653–644

    Article  Google Scholar 

  5. L.C. Pescatori, P. Torcia, L. Nicosia, G. Mauri, U.G. Rossi, M. Cariati, Which needle in the treatment of thyroid nodules? Gland Surg. 7(2), 111–116 (2018). https://doi.org/10.21037/gs.2018.01.03

    Article  PubMed  PubMed Central  Google Scholar 

  6. M. Melany, S. Chen, Thyroid cancer: ultrasound imaging and fine-needle aspiration biopsy. Endocrinol. Metab. Clin. North Am. 46(3), 691–711 (2017). https://doi.org/10.1016/j.ecl.2017.04.011

    Article  PubMed  Google Scholar 

  7. A.P. Mainini, C. Monaco, L.C. Pescatori, C. De Angelis, F. Sardanelli, L.M. Sconfienza, G. Mauri, Image-guided thermal ablation of benign thyroid nodules. J. Ultrasound 20(1), 11–22 (2017). https://doi.org/10.1007/s40477-016-0221-6

    Article  PubMed  Google Scholar 

  8. G. Mauri, L. Cova, C.G. Monaco, L.M. Sconfienza, S. Corbetta, S. Benedini, F. Ambrogi, V. Milani, A. Baroli, T. Ierace, L. Solbiati, Benign thyroid nodules treatment using percutaneous laser ablation (PLA) and radiofrequency ablation (RFA). Int. J. Hyperth. 15, 1–5 (2016). https://doi.org/10.1080/02656736.2016.1244707

    Article  CAS  Google Scholar 

  9. G. Mauri, L.M. Sconfienza, Percutaneous ablation holds the potential to substitute for surgery as first choice treatment for symptomatic benign thyroid nodules. Int. J. Hyperth. 22, 1–2 (2016). https://doi.org/10.1080/02656736.2016.1257827

    Article  Google Scholar 

  10. C.M. Pacella, G. Mauri, Is there a role for minimally invasive thermal ablations in the treatment of autonomously functioning thyroid nodules? Int. J. Hyperth. 34(5), 636–638 (2018). https://doi.org/10.1080/02656736.2018.1462537

    Article  Google Scholar 

  11. C.M. Pacella, G. Mauri, G. Achille, D. Barbaro, G. Bizzarri, P. De Feo, E. Di Stasio, R. Esposito, G. Gambelunghe, I. Misischi, B. Raggiunti, T. Rago, G.L. Patelli, S. D’Este, P. Vitti, E. Papini, Outcomes and risk factors for complications of laser ablation for thyroid nodules: a multicenter study on 1531 patients. J. Clin. Endocrinol. Metab. 100(10), 3903–3910 (2015). https://doi.org/10.1210/jc.2015-1964

    Article  CAS  PubMed  Google Scholar 

  12. C.M. Pacella, G. Mauri, R. Cesareo, V. Paqualini, R. Cianni, P. De Feo, G. Gambelunghe, B. Raggiunti, D. Tina, M. Deandrea, P.P. Limone, A. Mormile, M. Giusti, S. Oddo, G. Achille, E. Di Stasio, I. Misischi, E. Papini, A comparison of laser with radiofrequency ablation for the treatment of benign thyroid nodules: a propensity score matching analysis. Int. J. Hyperth. 33, 1–9 (2017). https://doi.org/10.1080/02656736.2017.1332395

    Article  Google Scholar 

  13. K. Wolinski, A. Stangierski, M. Ruchala, Comparison of diagnostic yield of core-needle and fine-needle aspiration biopsies of thyroid lesions: systematic review and meta-analysis. Eur. Radiol. 27(1), 431–436 (2017). https://doi.org/10.1007/s00330-016-4356-9

    Article  PubMed  Google Scholar 

  14. S. Gitto, G. Grassi, C. De Angelis, C.G. Monaco, S. Sdao, F. Sardanelli, L.M. Sconfienza, G. Mauri, A computer-aided diagnosis system for the assessment and characterization of low-to-high suspicion thyroid nodules on ultrasound. Radiol. Med. 124(2), 118–125 (2019). https://doi.org/10.1007/s11547-018-0942-z

    Article  PubMed  Google Scholar 

  15. M.C. Frates, C.B. Benson, J.W. Charboneau, E.S. Cibas, O.H. Clark, B.G. Coleman, J.J. Cronan, P.M. Doubilet, D.B. Evans, J.R. Goellner, I.D. Hay, B.S. Hertzberg, C.M. Intenzo, R.B. Jeffrey, J.E. Langer, P.R. Larsen, S.J. Mandel, W.D. Middleton, C.C. Reading, S.I. Sherman, F.N. Tessler, Society of Radiologists in Ultrasound: Management of thyroid nodules detected at US: Society of Radiologists in Ultrasound consensus conference statement. Radiology 237(3), 794–800 (2005). https://doi.org/10.1148/radiol.2373050220

    Article  PubMed  Google Scholar 

  16. H. Gharib, E. Papini, J.R. Garber, D.S. Duick, R.M. Harrell, L. Hegedus, R. Paschke, R. Valcavi, P. Vitti, AACE/ACE/AME Task Force on Thyroid Nodules, American Association of Clinical Endocrinologists, American College of Endocrinology, and Associazione Medici Endocrinologi Medical Guidelines for Clinical Practice for the Diagnosis and Management of Thyroid Nodules–2016 Update. Endocr. Pract. 22(5), 622–639 (2016). https://doi.org/10.4158/EP161208.GL

    Article  PubMed  Google Scholar 

  17. E.J. Ha, H.K. Lim, J.H. Yoon, J.H. Baek, K.H. Do, M. Choi, J.A. Choi, M. Lee, D.G. Na, Korean Society of Thyroid Radiology (KSThR) and Korean Society of Radiology, Primary imaging test and appropriate biopsy methods for thyroid nodules: Guidelines by Korean Society of Radiology and National Evidence-Based Healthcare Collaborating Agency. Korean J. Radiol. 19(4), 623–631 (2018). https://doi.org/10.3348/kjr.2018.19.4.623

    Article  PubMed  PubMed Central  Google Scholar 

  18. B.R. Haugen, E.K. Alexander, K.C. Bible, G.M. Doherty, S.J. Mandel, Y.E. Nikiforov, F. Pacini, G.W. Randolph, A.M. Sawka, M. Schlumberger, K.G. Schuff, S.I. Sherman, J.A. Sosa, D.L. Steward, R.M. Tuttle, L. Wartofsky, 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 26(1), 1–133 (2016). https://doi.org/10.1089/thy.2015.0020

    Article  PubMed  PubMed Central  Google Scholar 

  19. G. Russ, S.J. Bonnema, M.F. Erdogan, C. Durante, R. Ngu, L. Leenhardt, European Thyroid Association Guidelines for Ultrasound Malignancy Risk Stratification of Thyroid Nodules in Adults: the EU-TIRADS. Eur. Thyroid J. 6(5), 225–237 (2017). https://doi.org/10.1159/000478927

    Article  PubMed  PubMed Central  Google Scholar 

  20. J.H. Shin, J.H. Baek, J. Chung, E.J. Ha, J.H. Kim, Y.H. Lee, H.K. Lim, W.J. Moon, D.G. Na, J.S. Park, Y.J. Choi, S.Y. Hahn, S.J. Jeon, S.L. Jung, D.W. Kim, E.K. Kim, J.Y. Kwak, C.Y. Lee, H.J. Lee, J.H. Lee, J.H. Lee, K.H. Lee, S.W. Park, J.Y. Sung, Korean Society of Thyroid Radiology (KSThR) and Korean Society of Radiology, Ultrasonography diagnosis and imaging-based management of thyroid nodules: Revised Korean Society of Thyroid Radiology Consensus Statement and Recommendations. Korean J. Radiol. 17(3), 370–395 (2016). https://doi.org/10.3348/kjr.2016.17.3.370

    Article  PubMed  PubMed Central  Google Scholar 

  21. F.N. Tessler, W.D. Middleton, E.G. Grant, J.K. Hoang, L.L. Berland, S.A. Teefey, J.J. Cronan, M.D. Beland, T.S. Desser, M.C. Frates, L.W. Hammers, U.M. Hamper, J.E. Langer, C.C. Reading, L.M. Scoutt, A.T. Stavros, ACR Thyroid Imaging, Reporting and Data System (TI-RADS): White Paper of the ACR TI-RADS Committee. J. Am. Coll. Radiol. 14(5), 587–595 (2017). https://doi.org/10.1016/j.jacr.2017.01.046

    Article  PubMed  Google Scholar 

  22. T.M. Shaneyfelt, M.F. Mayo-Smith, J. Rothwangl, Are guidelines following guidelines? The methodological quality of clinical practice guidelines in the peer-reviewed medical literature. JAMA 281(20), 1900–1905 (1999)

    Article  CAS  Google Scholar 

  23. R. Grilli, N. Magrini, A. Penna, G. Mura, A. Liberati, Practice guidelines developed by specialty societies: the need for a critical appraisal. Lancet 355(9198), 103–106 (2000). https://doi.org/10.1016/S0140-6736(99)02171-6

    Article  CAS  PubMed  Google Scholar 

  24. F. Sardanelli, H. Bashir, D. Berzaczy, G. Cannella, A. Espeland, N. Flor, T. Helbich, M. Hunink, D.E. Malone, R. Mann, C. Muzzupappa, L.J. Petersen, K. Riklund, L.M. Sconfienza, Z. Serafin, S. Spronk, J. Stoker, E.J. van Beek, D. Vorwerk, G.D. Leo, The role of imaging specialists as authors of systematic reviews on diagnostic and interventional imaging and its impact on scientific quality: report from the EuroAIM Evidence-based Radiology Working Group. Radiology 272(2), 533–540 (2014). https://doi.org/10.1148/radiol.14131730

    Article  PubMed  Google Scholar 

  25. M.C. Brouwers, M.E. Kho, G.P. Browman, J.S. Burgers, F. Cluzeau, G. Feder, B. Fervers, I.D. Graham, J. Grimshaw, S.E. Hanna, P. Littlejohns, J. Makarski, L. Zitzelsberger, AGREE Next Steps Consortium: AGREE II: advancing guideline development, reporting and evaluation in health care. CMAJ 182(18), E839–842 (2010). https://doi.org/10.1503/cmaj.090449

    Article  PubMed  PubMed Central  Google Scholar 

  26. AGREE Next Steps Consortium: The AGREE II Instrument (2013). Retrieved from http://www.agreetrust.org/wp-content/uploads/2013/10/AGREE-II-Users-Manual-and-23-item-Instrument_2009_UPDATE_2013.pdf on 04/21/2017.

  27. C. Messina, B. Bignotti, A. Bazzocchi, C.M. Phan, A. Tagliafico, G. Guglielmi, F. Sardanelli, L.M. Sconfienza, A critical appraisal of the quality of adult dual-energy X-ray absorptiometry guidelines in osteoporosis using the AGREE II tool: an EuroAIM initiative. Insights Imaging 8(3), 311–317 (2017). https://doi.org/10.1007/s13244-017-0553-6

    Article  PubMed  PubMed Central  Google Scholar 

  28. N. Sekercioglu, R. Al-Khalifah, J.E. Ewusie, R.M. Elias, L. Thabane, J.W. Busse, N. Akhtar-Danesh, A. Iorio, T. Isayama, J.P. Martinez, I.D. Florez, G.H. Guyatt, A critical appraisal of chronic kidney disease mineral and bone disorders clinical practice guidelines using the AGREE II instrument. Int. Urol. Nephrol. 49(2), 273–284 (2017). https://doi.org/10.1007/s11255-016-1436-3

    Article  CAS  PubMed  Google Scholar 

  29. J.J. Armstrong, I.B. Rodrigues, T. Wasiuta, J.C. MacDermid, Quality assessment of osteoporosis clinical practice guidelines for physical activity and safe movement: an AGREE II appraisal. Arch. Osteoporos. 11, 6 (2016). https://doi.org/10.1007/s11657-016-0260-9

    Article  PubMed  Google Scholar 

  30. Y. Fang, L. Yao, J. Sun, J. Zhang, Y. Li, R. Yang, K. Yang, L. Tian, Appraisal of clinical practice guidelines on the management of hypothyroidism in pregnancy using the Appraisal of Guidelines for Research and Evaluation II instrument. Endocrine 60(1), 4–14 (2018). https://doi.org/10.1007/s12020-018-1535-2

    Article  CAS  PubMed  Google Scholar 

  31. C. Messina, B. Bignotti, A. Tagliafico, D. Orlandi, A. Corazza, F. Sardanelli, L.M. Sconfienza, A critical appraisal of the quality of adult musculoskeletal ultrasound guidelines using the AGREE II tool: an EuroAIM initiative. Insights Imaging 8(5), 491–497 (2017). https://doi.org/10.1007/s13244-017-0563-4

    Article  PubMed  PubMed Central  Google Scholar 

  32. Y. Ou, I. Goldberg, C. Migdal, P.P. Lee, A critical appraisal and comparison of the quality and recommendations of glaucoma clinical practice guidelines. Ophthalmology 118(6), 1017–1023 (2011). https://doi.org/10.1016/j.ophtha.2011.03.038

    Article  PubMed  Google Scholar 

  33. P. Perros, K. Boelaert, S. Colley, C. Evans, R.M. Evans, G. Gerrard Ba, J. Gilbert, B. Harrison, S.J. Johnson, T.E. Giles, L. Moss, V. Lewington, K. Newbold, J. Taylor, R.V. Thakker, J. Watkinson, G.R. Williams, British Thyroid Association, Guidelines for the management of thyroid cancer. Clin. Endocrinol. (Oxf.) 81(Suppl 1), 1–122 (2014). https://doi.org/10.1111/cen.12515

    Article  CAS  Google Scholar 

  34. Y.H. Lee, J.H. Baek, S.L. Jung, J.Y. Kwak, J.H. Kim, J.H. Shin,Korean Society of Thyroid Radiology (KSThR), Korean Society of Radiology, Ultrasound-guided fine needle aspiration of thyroid nodules: a consensus statement by the Korean Society of Thyroid Radiology. Korean J. Radiol. 16(2), 391–401 (2015). https://doi.org/10.3348/kjr.2015.16.2.391

    Article  PubMed  PubMed Central  Google Scholar 

  35. E. Vasse, M. Vernooij-Dassen, I. Cantegreil, M. Franco, P. Dorenlot, B. Woods, E. Moniz-Cook, Guidelines for psychosocial interventions in dementia care: a European survey and comparison. Int. J. Geriatr. Psychiatry 27(1), 40–48 (2012). https://doi.org/10.1002/gps.2687

    Article  CAS  PubMed  Google Scholar 

  36. L. Zeng, L. Zhang, Z. Hu, E.A. Ehle, Y. Chen, L. Liu, M. Chen, Systematic review of evidence-based guidelines on medication therapy for upper respiratory tract infection in children with AGREE instrument. PLoS ONE 9(2), e87711 (2014). https://doi.org/10.1371/journal.pone.0087711

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. T. Tejani, S. Mubeen, J. Seehra, M.T. Cobourne, An exploratory quality assessment of orthodontic clinical guidelines using the AGREE II instrument. Eur. J. Orthod. 30 39(6), 654–659 (2017). https://doi.org/10.1093/ejo/cjx017

    Article  Google Scholar 

  38. S.S. Ahn, E.K. Kim, D.R. Kang, S.K. Lim, J.Y. Kwak, M.J. Kim, Biopsy of thyroid nodules: comparison of three sets of guidelines. AJR Am. J. Roentgenol. 194(1), 31–37 (2010). https://doi.org/10.2214/AJR.09.2822

    Article  PubMed  Google Scholar 

  39. E.J. Ha, D.G. Na, J.H. Baek, J.Y. Sung, J.H. Kim, S.Y. Kang, US fine-needle aspiration biopsy for thyroid malignancy: diagnostic performance of Seven Society Guidelines applied to 2000 thyroid nodules. Radiology 287(3), 893–900 (2018). https://doi.org/10.1148/radiol.2018171074

    Article  PubMed  Google Scholar 

  40. W.D. Middleton, S.A. Teefey, C.C. Reading, J.E. Langer, M.D. Beland, M.M. Szabunio, T.S. Desser, Comparison of Performance Characteristics of American College of Radiology TI-RADS, Korean Society of Thyroid Radiology TIRADS, and American Thyroid Association Guidelines. AJR Am. J. Roentgenol. 210(5), 1148–1154 (2018). https://doi.org/10.2214/AJR.17.18822

    Article  PubMed  Google Scholar 

  41. T.W. Huang, J.H. Lai, M.Y. Wu, S.L. Chen, C.H. Wu, K.W. Tam, Systematic review of clinical practice guidelines in the diagnosis and management of thyroid nodules and cancer. BMC Med. 11, 191 (2013). https://doi.org/10.1186/1741-7015-11-191

    Article  PubMed  PubMed Central  Google Scholar 

  42. W. Hoffmann-Esser, U. Siering, E.A. Neugebauer, A.C. Brockhaus, U. Lampert, M. Eikermann, Guideline appraisal with AGREE II: systematic review of the current evidence on how users handle the 2 overall assessments. PLoS ONE 12(3), e0174831 (2017). https://doi.org/10.1371/journal.pone.0174831

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This work has been conducted within the framework of the Network for Assessment of Imaging in Medicine (EuroAIM), research platform of the European Institute for Biomedical Research under the umbrella of the European Society of Radiology (http://www.eibir.org/scientific-activities/joint-initiatives/euroaim/). F.S. is the chair of the EuroAIM, L.M.S. is the coordinator of the guideline appraisal project and all other authors are members of the EuroAIM. S.B., K.B. and R.K.L. are delegated members of the European Society of Head and Neck Radiology.

Author information

Authors and Affiliations

  1. Postgraduation School in Radiodiagnostics, Università degli Studi di Milano, Milano, Italy

    Salvatore Gitto, Ilaria Emili, Luca Nicosia & Lorenzo Carlo Pescatori

  2. Department of Neuroradiology, The National Hospital for Neurology and Neurosurgery, University College London Hospitals NHS Trust, London, UK

    Sotirios Bisdas

  3. Department of Brain Repair and Rehabilitation, Queen Square Institute of Neurology, London, UK

    Sotirios Bisdas

  4. Department of Radiology, Imperial College Healthcare NHS Trust, London, UK

    Kunwar Bhatia

  5. Department of Radiology, Northwick Park & Central Middlesex Hospitals, London North West University Healthcare NHS Trust, London, UK

    Ravi K. Lingam

  6. Servizio di Radiologia, IRCCS Policlinico San Donato, San Donato Milanese, Italy

    Francesco Sardanelli

  7. Dipartimento di Scienze Biomediche per la Salute, Università degli Studi di Milano, Milano, Italy

    Francesco Sardanelli & Luca Maria Sconfienza

  8. IRCCS Istituto Ortopedico Galeazzi, Milano, Italy

    Luca Maria Sconfienza

  9. Divisione di Radiologia Interventistica, IRCCS Istituto Europeo di Oncologia, Milano, Italy

    Giovanni Mauri

Authors
  1. Salvatore Gitto
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sotirios Bisdas
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ilaria Emili
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Luca Nicosia
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Lorenzo Carlo Pescatori
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Kunwar Bhatia
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Ravi K. Lingam
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Francesco Sardanelli
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Luca Maria Sconfienza
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Giovanni Mauri
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Salvatore Gitto.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Gitto, S., Bisdas, S., Emili, I. et al. Clinical practice guidelines on ultrasound-guided fine needle aspiration biopsy of thyroid nodules: a critical appraisal using AGREE II. Endocrine 65, 371–378 (2019). https://doi.org/10.1007/s12020-019-01898-w

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12020-019-01898-w

Keywords

Search

Navigation