Advertisement

Color Doppler ultrasonography diagnostic value in detection of malignant nodules in cysts with pathologically proven thyroid malignancy: a systematic review and meta-analysis

  • L. Darvish
  • M. Khezri
  • S. H. Teshnizi
  • N. Roozbeh
  • J. G. Dehkordi
  • A. AmraeeEmail author
Research Article
  • 10 Downloads

Abstract

Aims

Today, the color Doppler ultrasonography is used to further evaluate suspected malignant tumors. This study investigates the malignant thyroid nodules using color Doppler.

Methods

After extracting true positive, false positive, false negative, and true negative among included studies, a quality was evaluated by the Quality Assessment of Diagnostic Accuracy Studies-2 tool. Sensitivity, specificity, positive likelihood ratio, negative likelihood ratio, and diagnostic odds ratio (with 95% confidence interval) were found using a random effect model. Summary receiver operating characteristic curves (SROC) were used to assess relationship between sensitivity and specificity. The area under the curve of the SROC was calculated to estimate the performance of color Doppler ultrasound to distinguish malignant thyroid nodules. Our registration code in PROSPERO is CRD42018111198.

Results

Of 1125 articles, 288 articles were selected for the further investigation. After excluding irrelevant and poor articles, 20 studies were included for the meta-analysis. According to a random effect model, the pooled sensitivity and specificity of color Doppler ultrasound to distinguish malignant thyroid nodules were estimated as 0.74 (95% CI 0.62–0.83; \( I^{2} = 89.94\% \)) and 0.70 (95% CI 0.56–0.81; \( I^{2} = 97.79\% \)), respectively. The SROC curve consists of representing the paired results for sensitivity and specificity. According to SROC, AUC = 0.78 (95% CI 0.74–0.81) is between 0.75 and 0.92, so that color Doppler ultrasound has a good accuracy.

Conclusion

Color Doppler is a valuable non-invasive method for evaluating thyroid nodules, and it is a high-sensitivity diagnostic tool for assessing thyroid nodules. Resistive index > 0.75 and a pattern III or more in color Doppler predicts malignant with the confidence. Due to its precision, cost-efficiency, easy access, and non-invasive nature, color Doppler should be included in the standard clinical protocol for the decision-making period and the treatment evaluation.

Keywords

Color Doppler ultrasound Thyroid nodule Malignant thyroid nodule FNA 

Notes

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval (research involving human participants and/or animals)

This work has no human or animal participants.

Informed consent

There is no consent for this work.

References

  1. 1.
    Popoveniuc G, Jonklaas J. Thyroid nodules. Med Clin North Am. 2012;96(2):329–49.Google Scholar
  2. 2.
    Ezzat S, Sarti DA, Cain DR, et al. Thyroid incidentalomas. Prevalence by palpation and ultrasonography. Arch Int Med. 1994;154(16):1838–40.Google Scholar
  3. 3.
    Acar T, Ozbek SS, Acar S. Incidentally discovered thyroid nodules: frequency in an adult population during Doppler ultrasonographic evaluation of cervical vessels. Endocrine. 2014;45(1):73–8.Google Scholar
  4. 4.
    Miki H, Oshimo K, Inoue H, et al. Incidence of ultrasonographically detected thyroid nodules in healthy adults. Tokushima J Exp Med. 1993;40(1–2):43–6.Google Scholar
  5. 5.
    Varverakis E, Neonakis E, Tzardi M, et al. Role of color Doppler ultrasonography in the preoperative management of cold thyroid nodules. Hormones. 2007;6(1):44–51.Google Scholar
  6. 6.
    Miyakawa M, Onoda N, Etoh M, et al. Diagnosis of thyroid follicular carcinoma by the vascular pattern and velocimetric parameters using high resolution pulsed and power Doppler ultrasonography. Endocr J. 2005;52(2):207–12.Google Scholar
  7. 7.
    Garber J. Thyroid Nodules 2006: managing what has been known for over 50 years. Hormones. 2006;5(3):179–86.Google Scholar
  8. 8.
    Yassa L, Cibas ES, Benson CB, et al. Long-term assessment of a multidisciplinary approach to thyroid nodule diagnostic evaluation. Cancer. 2007;111(6):508–16.Google Scholar
  9. 9.
    Yang J, Schnadig V, Logrono R, et al. Fine-needle aspiration of thyroid nodules: a study of 4703 patients with histologic and clinical correlations. Cancer. 2007;111(5):306–15.Google Scholar
  10. 10.
    Nayar R, Ivanovic M. 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. 2009;117(3):195–202.Google Scholar
  11. 11.
    Wolinski K, Stangierski A, Ruchala M. Comparison of diagnostic yield of core-needle and fine-needle aspiration biopsies of thyroid lesions: systematic review and meta-analysis. Eur Radiol. 2017;27(1):431–6.Google Scholar
  12. 12.
    Sharma R, Chakravarty KL, Tripathi M, et al. Role of 99mTc Tetrofosmin delayed scintigraphy and color Doppler sonography in characterization of solitary thyroid nodules. Nucl Med Commun. 2007;28(11):847–51.Google Scholar
  13. 13.
    Papini E, Guglielmi R, Bianchini A, et al. Risk of malignancy in nonpalpable thyroid nodules: predictive value of ultrasound and color-Doppler features. J Clin Endocrinol Metab. 2002;87(5):1941–6.Google Scholar
  14. 14.
    Kang HW, No JH, Chung JH, et al. Prevalence, clinical and ultrasonographic characteristics of thyroid incidentalomas. Thyroid. 2004;14(1):29–33.Google Scholar
  15. 15.
    Kim E, Park CS, Chung WY, et al. New sonographic criteria for recommending fine-needle aspiration biopsy of non-palpable solid nodules of the thyroid. Am J Roentgenol. 2002;178(3):687–91.Google Scholar
  16. 16.
    Frates MC, Benson CB, Doubilet PM, et al. Can color Doppler sonography aid in the prediction of malignancy of thyroid nodules? J Ultrasound Med. 2003;22(2):127–31.Google Scholar
  17. 17.
    Iared W, Shigueoka DC, Cristófoli JC, et al. Use of color Doppler ultrasonography for the prediction of malignancy in follicular thyroid neoplasms: systematic review and meta analysis. J Ultrasound Med. 2010;29(3):419–25.Google Scholar
  18. 18.
    Whiting PF, Rutjes AW, Westwood ME, et al. QUADAS-2: a revised tool for the quality assessment of diagnostic accuracy studies. Ann Intern Med. 2011;155(8):529–36.Google Scholar
  19. 19.
    Jones CM, Athanasiou T. Summary receiver operating characteristic curve analysis techniques in the evaluation of diagnostic tests. Ann Thorac Surg. 2005;79:16–20.Google Scholar
  20. 20.
    Ebeed AE, Romeih MA, Refat MM, et al. Role of ultrasound, color doppler, elastography and micropure imaging in differentiation between benign and malignant thyroid nodules. Egypt J Radiol Nucl Med. 2017;48(3):603–10.Google Scholar
  21. 21.
    Appetecchia M, Solivetti FM. The association of colour flow Doppler sonography and conventional ultrasonography improves the diagnosis of thyroid carcinoma. Horm Res. 2006;66(5):249–56.Google Scholar
  22. 22.
    Bozbora A, Erbil Y, Ozarmagan S, et al. Color Doppler sonography in cold thyroid nodules for malignancy prediction. Acta Chir Belg. 2002;102(4):259–62.Google Scholar
  23. 23.
    Fukunari N, Nagahama M, Sugino K, et al. Clinical evaluation of color Doppler imaging for the differential diagnosis of thyroid follicularlesions. World J Surg. 2004;28(12):1261–5.Google Scholar
  24. 24.
    Kim DW, In HS, Choo HJ, et al. Solid and isoechoic thyroid nodules without malignant sonographic features: comparison of malignancy rate according to nodule size, shape and color Doppler pattern. Ultrasound Med Biol. 2013;39(2):269–74.Google Scholar
  25. 25.
    Rao G, Rao S, Varma R, et al. Predicting malignancy in a solitary thyroid nodule: a prospective study on the role of color Doppler Ultrasonography. Otorhinolaryngol Clin. 2014;6(1):9–14.Google Scholar
  26. 26.
    Tatar IG, Kurt A, Yilmaz KB, et al. The role of elastosonography, gray-scale and colour flow Doppler sonography in prediction of malignancy in thyroid nodules. Radiol Oncol. 2014;48(4):348–53.Google Scholar
  27. 27.
    Yuan WH, Chiou HJ, Chou YH, et al. Gray scale and color Doppler ultrasonographic manifestations of papillary thyroid carcinoma: analysis of 51 cases. Clin Imaging. 2006;30(6):394–401.Google Scholar
  28. 28.
    Iannuccilli JD, Cronan JJ, Monchik JM. Risk for malignancy of thyroid nodules as assessed by sonographic criteria: the need for biopsy. J Ultrasound Med. 2004;23(11):1455–64.Google Scholar
  29. 29.
    Stacul F, Bertolotto M, De Gobbis F, et al. US, colour-Doppler US and fine-needle aspiration biopsy in the diagnosis of thyroid nodules. Radiol Med. 2007;112(5):751–62.Google Scholar
  30. 30.
    Brunese L, Romeo A, Iorio S, et al. A new marker for diagnosis of thyroid papillary cancer: B-flow twinkling sign. J Ultrasound Med. 2008;27(8):1187–94.Google Scholar
  31. 31.
    De Nicola H, Szejnfeld J, Logullo AF, et al. Flow pattern and vascular resistive index as predictors of malignancy risk in thyroid follicularneoplasms. J Ultrasound Med. 2005;24(7):897–904.Google Scholar
  32. 32.
    Sultan LR, Xiong H, Zafar HM, et al. Vascularity assessment of thyroid nodules by quantitative color Doppler ultrasound. Ultrasound Med Biol. 2015;41(5):1287–93.Google Scholar
  33. 33.
    Singh D, Makwan M, Verma GL, et al. Evaluation of thyroid nodules by Gray scale and Doppler sonography and correlation with fine needle aspiration cytology. Int Sur J. 2017;4(7):2197–204.Google Scholar
  34. 34.
    Berni A, Tromba L, Falvo L, et al. Malignant thyroid nodules: comparison between color Doppler diagnosis and histological examination of surgical samples. Chir Ital. 2002;54(5):643–7.Google Scholar
  35. 35.
    Gannon AW, Langer JE, Bellah RJ, et al. Diagnostic accuracy of ultrasound with color flow doppler in children with thyroid nodules. Clin Endocrinol Metab. 2018;103(5):1958–65.Google Scholar
  36. 36.
    Salehi M, Nalaini F, Izadi B, et al. Gray-scale vs. color doppler ultrasound in cold thyroid nodules. Glob J Health Sci. 2014;7(3):147–52.Google Scholar
  37. 37.
    Palaniappan MK, Aiyappan SK, Ranga U. Role of gray scale, color Doppler and spectral Doppler in differentiation between malignant and benign thyroid nodules. J Clin Diagn Res. 2016;10(8):TC01–6.Google Scholar
  38. 38.
    Ma JJ, Ding H, Xu BH, et al. Diagnostic performances of various gray-scale, color Doppler, and contrast-enhanced ultrasonography findings in predicting malignant thyroid nodules. Thyroid. 2014;24(2):355–63.Google Scholar
  39. 39.
    Kalantari S. The diagnostic value of color Doppler ultrasonography in predicting thyroid nodules malignancy. Int Tinnitus J. 2018;22(1):35–9.Google Scholar
  40. 40.
    Cantisani V, Catania A, De Antoni E, et al. Is pattern III as evidenced by US color-Doppler useful in predicting thyroid nodule malignancy? Large-scale retrospective analysis. Clin Ter. 2010;161(2):e49–52.Google Scholar
  41. 41.
    Titton RL, Gervais DA, Boland GW, et al. Sonography and sonographically guided fine-needle aspiration biopsy of the thyroid gland: indications and techniques, pearls and pitfalls. Am J Roentgenol. 2003;181(1):267–71.Google Scholar
  42. 42.
    Wienke JR, Chong WK, Fielding JR, et al. Sonographic features of benign thyroid nodules: interobserver reliability and overlap with malignancy. J Ultrasound Med. 2003;22(10):102731.Google Scholar
  43. 43.
    Lu C, Chang TC, Hsiao YL, et al. Ultrasonographic findings of papillary thyroid carcinoma and their relation to pathologic changes. J Formos Med Assoc. 1994;93(11–12):933–8.Google Scholar
  44. 44.
    Solbiati L, Volterrani L, Rizzatto G. The thyroid gland with low uptake lesions: evaluation by ultrasound. Radiology. 1985;155(1):187–91.Google Scholar
  45. 45.
    Liebeshind A, Sikora AG, Komisar A, et al. Rates of malignancy in incidentally discovered thyroid nodules evaluated with sonography and fine-needle aspiration. J Ultrasound Med. 2005;24(5):629–34.Google Scholar
  46. 46.
    Ross DS. Nonpalpable thyroid nodules—managing an epidemic. J Clin Endocrinol Metab. 2002;87(5):1938–40.Google Scholar
  47. 47.
    Bakhshaee M, Davoudi Y, Mehrabi M, et al. Vascular pattern and spectral parameters of power Doppler ultrasound as predictors of malignancy risk in thyroid nodules. Laryngoscope. 2008;118(12):2182–6.Google Scholar
  48. 48.
    Rago T, Vitti P, Chiovato L, et al. Role of conventional ultrasonography and colour flow Doppler sonography in predicting malignancy in ‘cold’ thyroid nodules. Eur J Endocrinol. 1998;138(1):41–6.Google Scholar
  49. 49.
    Moon HJ, Kwak JY, Kim MJ, et al. Can vascularity at power Doppler US help predict thyroid malignancy? Radiology. 2010;255(1):260–9.Google Scholar
  50. 50.
    Argalia G, D’Ambrosio F, Lucarelli F, et al. Echo Doppler in the characterization of thyroid nodular disease. Radiol Med. 1995;89(5):651–7.Google Scholar
  51. 51.
    Tamsel S, Demirpolat G, Erdogan M, et al. Power Doppler US patterns of vascularity and spectral Doppler US parameters in predicting malignancy in thyroid nodules. Clin Radiol. 2007;62(3):245–51.Google Scholar
  52. 52.
    Rosario PW, Silva AL, Borges MA, et al. Is Doppler ultrasound of additional value to gray-scale ultrasound in differentiating malignant and benign thyroid nodules? Arch Endocrinol Metab. 2015;59(1):79–83.Google Scholar
  53. 53.
    Clark KJ, Cronan JJ, Scola FH. Color Doppler sonography: anatomic and physiologic assessment of the thyroid. J Clin Ultrasound. 1995;23(4):215–23.Google Scholar
  54. 54.
    Wong KT, Ahuja AT. Ultrasound of thyroid cancer. Cancer Imaging. 2005;5(1):157–66.Google Scholar
  55. 55.
    Brown CL. Pathology of the cold nodule. Clin Endocrinol Metab. 1981;10(2):235–45.Google Scholar

Copyright information

© Federación de Sociedades Españolas de Oncología (FESEO) 2019

Authors and Affiliations

  1. 1.Mother and Child Welfare Research CenterHormozgan University of Medical SciencesBandar AbbasIran
  2. 2.Department of Radiology, Faculty of ParamedicineHormozgan University of Medical SciencesBandar AbbasIran
  3. 3.Hormozgan University of Medical SciencesBandar AbbasIran
  4. 4.Paramedical SchoolHormozgan University of Medical SciencesBandar AbbasIran
  5. 5.Social Determinants of Health Research CenterShahrekord University of Medical SciencesShahrekordIran
  6. 6.Department of Medical Physics, Faculty of Medicine, School of MedicineIran University of Medical SciencesTehranIran

Personalised recommendations