Journal of Zhejiang University SCIENCE B

, Volume 14, Issue 3, pp 195–206 | Cite as

Is there a real diagnostic impact of elastosonography and contrast-enhanced ultrasonography in the management of thyroid nodules?

  • Massimo Giusti
  • Davide Orlandi
  • Giulia Melle
  • Barbara Massa
  • Enzo Silvestri
  • Francesco Minuto
  • Gianni Turtulici
Article

Abstract

Ultrasonography (US) and the new applications US elastography (USE) and contrast-enhanced US (CEUS) are used in the screening of thyroid nodules, for which fine-needle aspiration biopsy (FNAB) is the best single diagnostic test. The aim of the study was to compare the sensitivity, specificity, positive predictive value (PPV), and accuracy of the four examinations in nodules with cytological and histological diagnoses. The study used data from US, FNAB, USE (elasticity (ELX 2/1) index), and CEUS (Peak index and time to peak (TTP) index) evaluated in 73 thyroid nodules in 63 consecutive patients likely to undergo surgery. Cytological-histological correlation was available for 38 nodules. No correlation emerged between nodule size and cytological results. A significant (P=0.03) positive correlation between cumulative US findings and cytological results was found. In addition, significant correlations between cumulative US findings and cytology (P=0.02) and between cumulative US findings and histology (P<0.0001) were found. US showed the best specificity and PPV, and FNAB the best sensitivity. There was no significant difference in the ELX 2/1 index, Peak index, or TTP index among nodules subdivided according to cytological scores. No significant correlation was found between ELX 2/1 index, Peak index, and TTP index, on the one hand, and nodule size, US cumulative findings, cytology, and histology on the other hand. The sensitivity of the ELX 2/1 index was high, but its specificity was very low. The accuracy and PPV of USE were lower than those of the other procedures. Only the correlation between Peak index and cumulative US findings reached a value close to significance. Our ultimate aim is to minimise unnecessary thyroidectomy. US and FNAB continue to play a central diagnostic role. The use of a US score showed high specificity and PPV. The specificity of FNAB was low in this selected series because of the numbers of indeterminate cytological responses. USE and CEUS are innovative techniques that need to be standardized. The ELX 2/1 index, Peak index, and TTP index seem to be unrelated to histology. The best statistical data on USE and CEUS concerned their sensitivity and PPV, respectively. At present, USE and CEUS are too time-consuming and of limited utility in selecting patients for surgery.

Key words

Thyroid nodules Cytology Histology Ultrasonography Elastosonography Contrast-enhanced ultrasonography 

CLC number

R581 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Argalia, G., de Bernardis, S., Mariani, D., Abbattista, T., Taccaliti, A., Ricciarelli, L., Faragona, S., Gusella, P.M., Giuseppetti, G.M., 2002. Ultrasonographic contrast agent: evaluation of time intensity curve in the characterisation of solitary thyroid nodules. Radiol. Med., 103(4): 407–413.PubMedGoogle Scholar
  2. Baloch, Z., LiVolsi, V.A., Jain, P., Jain, R., Aljada, I., Mandel, S., Langer, J.E., Gupta, P.K., 2003. Role of repeat fine-needle aspiration biopsy (FNAB) in the management of thyroid nodules. Diagn. Cytopathol., 29(4):203–206. [doi:10.1002/dc.10361]PubMedCrossRefGoogle Scholar
  3. Bartolazzi, A., Orlandi, F., Maggiorato, E., Volante, M., Arecco, F., Rossetto, R., Palestrini, N., Ghigo, E., Capotti, M., Bussolanti, G., et al., 2008. Galectin-3-expression analysis in the surgical selection of follicular thyroid nodules with indeterminate fine-needle aspiration cytology: a prospective multicentre study. Lancet Oncol., 9(6):543–549. [doi:10.1016/S1470-2045(08)70132-3]PubMedCrossRefGoogle Scholar
  4. Bartolotta, T.V., Midiri, M., Quaia, E., Bertolotto, M., Galia, M., Cademartiri, F., Legalla, R., Cardinale, A.E., 2005. Benign focal liver lesions: spectrum of findings on SonoVue-enhanced pulse-inversion ultrasonography. Eur. Radiol., 15(8):1643–1649. [doi:10.1007/s00330-005-2668-2]PubMedCrossRefGoogle Scholar
  5. Bartolotta, T.V., Midiri, M., Galia, M., Runza, G., Attard, M., Savoia, G., Lagalla, R., Cardinale, A.E., 2006. Qualitative and quantitative evaluation of solitary thyroid nodules with contrast-enhanced ultrasound; initial results. Eur. Radiol., 16(10):2234–2241. [doi:10.1007/s00330-006-0229-y]PubMedCrossRefGoogle Scholar
  6. British Thyroid Association, 2007. Guidelines for the Management of Thyroid Cancer in Adults. Royal College of Physicians of London and the British Thyroid Association, London. Available from http://www.british-thyroid-association.org Google Scholar
  7. Burch, H.B., 1995. Evaluation and management of the solid nodule. Endocrinol. Metab. Clin. North Am., 24(4): 663–710.PubMedGoogle Scholar
  8. Cakir, B., Aydin, C., Koruklouglu, B., Ozdemir, D., Sisman, L.C., Tuzun, D., Oguz, A., Guler, G., Guney, G., Kusdemir, A., et al., 2011. Diagnostic value of elastosonographically determined strain index in the differential diagnosis of benignant and malignant thyroid nodules. Endocrine, 39(1):89–98. [doi:10.1007/s12020-010-9416-3]PubMedCrossRefGoogle Scholar
  9. Castro, M.R., Gharib, H., 2003. Thyroid fine-needle aspiration biopsy: progress, practice, and pitfalls. Endocr. Pract., 9(2):128–136.PubMedGoogle Scholar
  10. Chow, L.S., Gharib, H., Goellner, J.R., van Heerden, J.A., 2001. Nondiagnostic thyroid fine-needle aspiration biopsy aspiration cytology: management dilemmas. Thyroid, 11(12):1147–1151. [doi:10.1089/1050725015274 0993]PubMedCrossRefGoogle Scholar
  11. Danese, D., Schiaccitano, S., Farsetti, A., Andreoli, M., Pontecorvi, A., 1998. Diagnostic accuracy of conventional versus sonography-guided fine-needle aspiration biopsy of thyroid nodules. Thyroid, 8(1):15–21. [doi:10.1089/thy. 1998.8.15]PubMedCrossRefGoogle Scholar
  12. Foppiani, L., Tancredi, M., Ansaldo, G.L., Ceppa, P., Aurati, L., Torre, G.C., Minuto, F., Giusti, M., 2003. Absence of histological malignancy in a patient cohort with follicular lesion on fine-needle aspiration. J. Endocrinol. Invest., 26(1):29–34.PubMedGoogle Scholar
  13. Friedrich-Rust, M., Sperber, A., Holzer, K., Diener, J., Grunwald, F., Badenhoop, K., Weber, S., Kriener, S., Hermann, E., Bechstein, W.O., et al., 2010. Real-time elastography and contrast-enhanced ultrasound for the assessment of thyroid nodules. Exp. Clin. Endocrinol. Diabetes, 118(9):602–609. [doi:10.1055/s-0029-1237701]PubMedCrossRefGoogle Scholar
  14. Garcia-Pascual, L., Barahona, M.J., Balsells, M., del Pozo, C., Anglada-Barcelo, J., Casalots-Casado, J., Veloso, E., Torres, J., 2011. Complex thyroid nodules with nondiagnostic fine needle aspiration cytology: histopathologic outcomes and comparison of the cytological variants (cystic vs. acellular). Endocrine, 39(1):33–40. [doi:10.1007/s12020-010-9409-2]PubMedCrossRefGoogle Scholar
  15. Gharib, H., Papini, E., 2007. Thyroid nodules: clinical importance, assessment, and treatment. Endocrinol. Metab. Clin. North Am., 36(3):707–735. [doi:10.1016/j.ecl. 2007.04.009]PubMedCrossRefGoogle Scholar
  16. Gharib, H., Papini, E., Valcalvi, R., Baskin, H.J., Crescenzi, A., Dottorini, M.E., Duick, D.S., Guglielmi, R., Hamilton, C.R. Jr., Zeiger, M.A., et al., 2006. American Association of Clinical Endocrinologists and Associazione Medici Endocrinologi medical guidelines for clinical practice for the diagnosis and management of thyroid nodules. Endocr. Pract., 12(1):63–102.PubMedGoogle Scholar
  17. Gomez Saez, J.M., 2010. Diagnostic usefulness of tumor markers in the thyroid cytological samples extracted by fine-needle aspiration biopsy. Endocr. Metab. Immune Disord. Drug Targets, 10(1):47–56. [doi:10.2174/187153010790828000]PubMedCrossRefGoogle Scholar
  18. Heidinger, C.H.R., Sobin, L.H., 1974. Histological Typing of Thyroid Tumors. In: Roto Satag, A.S. (Ed.), International Histological Classification of Tumors. Vol. 11, World Health Organization, Geneva, p.17–27.Google Scholar
  19. Henrichsen, T.L., Reading, C.C., 2011. Thyroid ultrasonography. Part 2: nodules. Radiol. Clin. North Am., 49(3): 417–424. [doi:10.1016/j.rcl.2011.02.003]PubMedCrossRefGoogle Scholar
  20. Horvath, E., Majlis, S., Rossi, R., Franco, C., Niedmann, J.P., Castro, A., Dominguez, M., 2009. An ultrasonogram reporting system for thyroid nodules stratifying cancer risk for clinical management. J. Clin. Endocrinol. Metab., 94(5):1748–1751. [doi:10.1210/jc.2008-1724]PubMedCrossRefGoogle Scholar
  21. Kim, D.W., Lee, E.J., Kim, S.H., Kim, T.H., Lee, S.H., Kim, D.H., Rho, M.H., 2009. Ultrasound-guided fine-needle aspiration biopsy of thyroid nodules: comparison in efficacy according to nodule size. Thyroid, 19(1):27–31. [doi:10.1089/thy.2008.0106]PubMedCrossRefGoogle Scholar
  22. Kim, E.K., Park, C.S., Chung, W.Y., Oh, K.K., Kim, D.I., Lee, J.T., Yoo, H.S., 2002. New sonographic criteria for recommending fine-needle aspiration biopsy of nonpalpable solid nodules of the thyroid. AJR Am. J. Roentgenol., 178(3):687–691.PubMedCrossRefGoogle Scholar
  23. Kim, E.S., Nam-Goong, I.S., Gong, G., Hong, S.J., Kim, W.B., Shong, Y.K., 2003. Postoperative findings and risk for malignancy in thyroid nodules with cytological diagnosis of so-called “follicular neoplasm”. Korean J. Intern. Med., 18(2):94–97.PubMedGoogle Scholar
  24. Layfield, L.J., Cibas, E.S., Gharib, H., Mandel, S.J., 2009. Thyroid aspiration cytology: current status. CA Cancer J. Clin., 59(2):99–110. [doi:10.3322/caac.20014]PubMedCrossRefGoogle Scholar
  25. Lewis, C.M., Chang, K.P., Pitman, M., Faquin, W.C., Randolph, G.W., 2009. Thyroid fine-needle aspiration biopsy: variability in reporting. Thyroid, 19(7):717–723. [doi:10.1089/thy.2008.0425]PubMedCrossRefGoogle Scholar
  26. Lippolis, P.V., Tognini, S., Materazzi, G., Polini, A., Mancini, R., Ambrosini, C.E., Dardano, A., Basolo, F., Seccia, M., Miccoli, P., et al., 2011. Is elastography actually useful in the presurgical selection of thyroid nodules with indeterminate cytology? J. Clin. Endocrinol. Metab., 96(11): E1826–E1830. [doi:10.1210/jc.2011-1021]PubMedCrossRefGoogle Scholar
  27. Lyshchik, A., Higashi, T., Asato, R., Tenaka, S., Ito, J., Mai, J.J., Pellot-Barakat, C., Insana, M.F., Brill, A.B., Saga, T., et al., 2005. Thyroid gland tumor diagnosis at US elastography. Radiology, 237(1):202–211. [doi:10.1148/radiol. 2363041248]PubMedCrossRefGoogle Scholar
  28. Massaro, F., Dolcino, M., Degrandi, R., Ferone, D., Mussap, M., Minuto, F., Giusti, M., 2009. Calcitonin assay in wash-out fluid after fine-needle aspiration biopsy in patients with a thyroid nodule and border-line value of the hormone. J. Endocrinol. Invest., 32(4):308–312.PubMedGoogle Scholar
  29. Mihai, R., Parker, A.J., Roskell, D., Sadler, G.P., 2009. One in four patients with follicular thyroid cytology (THY 3) has a thyroid carcinoma. Thyroid, 19(1):33–37. [doi:10.1089/thy.2008.0200]PubMedCrossRefGoogle Scholar
  30. Molinari, F., Mantovani, A., Deandrea, M., Limone, P., Garberoglio, R., Suri, J.S., 2010. Characterization of a single thyroid nodule by contrast-enhanced 3-D ultrasound. Ultrasound Med. Biol., 36(10):1616–1625. [doi:10.1016/j. ultrasmedbio.2010.07.011]PubMedCrossRefGoogle Scholar
  31. Moon, W.J., Baek, J.H., Jung, S.L., Kim, D.W., Kim, E.K., Kim, J.Y., Kwak, J.Y., Lee, J.H., Lee, J.H., Lee, Y.H., et al., 2011. Ultrasonography and the ultrasound-based management of thyroid nodules: consensus statement and recommendations. Korean J. Radiol., 12(1):1–14. [doi:10.3348/kjr.2011.12.1.1]PubMedCrossRefGoogle Scholar
  32. Nam-Goong, I.S., Kim, H.Y., Gong, G., Lee, H.K., Hong, S.J., Kim, W.B., Shong, Y.K., 2004. Ultrasonography-guided fine-needle aspiration of thyroid incidentaloma: correlation with pathological findings. Clin. Endocrinol. (Oxf.), 60(1):21–28. [doi:10.1046/j.1365-2265.2003.01912.x]CrossRefGoogle Scholar
  33. Nayar, R., Ivanovic, M., 2009. The indeterminate thyroid fine-needle aspiration. Cancer Cytopathol., 117(3): 195–202. [doi:10.1002/cncy.20029]CrossRefGoogle Scholar
  34. Nikiforova, M.N., Kimura, E.T., Gandhi, M., Biddinger, P.W., Knauf, J.A., Basolo, F., Zhu, Z., Giannini, R., Salvatore, G., Fusco, A., et al., 2003. BRAF mutations in thyroid tumors are restricted to papillary carcinoma and anaplastic or poorly differentiated carcinomas arising from papillary carcinomas. J. Clin. Endocrinol. Metab., 88(11): 5399–5404. [doi:10.1210/jc.2003-030838]PubMedCrossRefGoogle Scholar
  35. Rago, T., di Coscio, G., Basolo, F., Scutari, M., Elisei, R., Berti, P., Miccoli, R., Romani, R., Faviana, P., Pinchera, A., et al., 2007. Combined clinical, thyroid ulltrasound and cytological features help to predict thyroid malignancy in follicular and Hurthle cell thyroid lesions: results from a series of 505 consecutive patients. Clin. Endocrinol. (Oxf.), 66(1):13–20. [doi:10.1111/j.1365-2265. 2006.02677.x]Google Scholar
  36. Rago, T., Scutari, M., Santini, F., Loiacono, V., Piaggi, P., di Coscio, G., Basolo, F., Berti, P., Pinchera, A., Vitti, P., 2010. Real-time elastosonography: useful tool for refining the presurgical diagnosis in thyroid nodules with indeterminate or nondiagnostic cytology. J. Clin. Endocrinol. Metab., 95(12):5274–5280. [doi:10.1210/jc. 2010-0901]PubMedCrossRefGoogle Scholar
  37. Redman, R., Zalaznick, H., Mazzaferri, E.L., Massoll, N.A., 2006. The impact of assessing specimen adequacy and number of needle passes for fine-needle aspiration biopsy of thyroid nodules. Thyroid, 16(1):55–60. [doi:10.1089/thy.2006.16.55]PubMedCrossRefGoogle Scholar
  38. Rubaltelli, L., Corradin, S., Dorigo, A., Stabilito, M., Tregnaghi, A., Borsato, S., Stramare, R., 2009. Differential diagnosis of benignant and malignant thyroid nodules at elastosonography. Ultraschall Med., 30(2):175–179. [doi:10.1055/s-2008-1027442]PubMedCrossRefGoogle Scholar
  39. Sidoti, M., Marino, G., Resmini, E., Augeri, C., Cappi, C., Cavallero, D., Lagasio, C., Ceppa, P., Minuto, F., Giusti, M., 2006. The rationale use of fine needle aspiration biopsy (FNAB) in diagnosing thyroid nodules. Minerva Endocrinol., 31(2):159–172.PubMedGoogle Scholar
  40. Spiezia, S., Farina, R., Cerbone, G., Assanti, A.P., Iovino, V., Siciliani, M., Lombardi, G., Colao, A., 2001. Analysis of color Doppler signal intensity variation after levovist injection: a new approach to the diagnosis of thyroid nodules. J. Ultrasound Med., 20(3):223–231.PubMedGoogle Scholar
  41. Ueno, E., Ito, A., 2004. Diagnosis of breast cancer by elasticity imaging. Eizo Joho Med., 36(12):2–6.Google Scholar
  42. Vorlander, C., Wolf, J., Saalablan, S., Lienenluke, R.H., Wahl, R.A., 2010. Real-time ultrasound elastography—a non-invasive diagnostic procedure for evaluating dominant thyroid nodules. Langenbeck’s Arch. Surg., 395(7):865–871. [doi:10.1007/s00423-010-0685-3]CrossRefGoogle Scholar
  43. Yang, J., Schnadig, V., Logrono, R., Wasserman, P.G., 2007. Fine-needle aspiration for thyroid nodules: a study of 4703 patients with histological and clinical correlations. Cancer, 111(5):306–315. [doi:10.1002/cncr.22955]PubMedCrossRefGoogle Scholar
  44. Zhang, B., Jiang, Y.X., Liu, J.B., Yang, M., Dai, Q., Zhu, Q.L., Gao, P., 2010. Utility of contrast-enhanced ultrasound for evaluation of thyroid nodules. Thyroid, 20(1):51–57. [doi:10.1089/thy.2009.0045]PubMedCrossRefGoogle Scholar

Copyright information

© Zhejiang University and Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Massimo Giusti
    • 1
  • Davide Orlandi
    • 2
  • Giulia Melle
    • 1
  • Barbara Massa
    • 3
  • Enzo Silvestri
    • 2
  • Francesco Minuto
    • 1
  • Gianni Turtulici
    • 2
  1. 1.Endocrine UnitSan Martino University HospitalGenoaItaly
  2. 2.Radiology UnitEvangelico HospitalGenoaItaly
  3. 3.Cytopathology and Pathology UnitSan Martino University HospitalGenoaItaly

Personalised recommendations