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

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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.

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References

  1. Popoveniuc G, Jonklaas J. Thyroid nodules. Med Clin North Am. 2012;96(2):329–49.

    CAS  PubMed  PubMed Central  Google Scholar 

  2. Ezzat S, Sarti DA, Cain DR, et al. Thyroid incidentalomas. Prevalence by palpation and ultrasonography. Arch Int Med. 1994;154(16):1838–40.

    CAS  Google Scholar 

  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.

    CAS  PubMed  Google Scholar 

  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.

    CAS  PubMed  Google Scholar 

  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.

    PubMed  Google Scholar 

  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.

    PubMed  Google Scholar 

  7. Garber J. Thyroid Nodules 2006: managing what has been known for over 50 years. Hormones. 2006;5(3):179–86.

    PubMed  Google Scholar 

  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.

    PubMed  Google Scholar 

  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.

    PubMed  Google Scholar 

  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.

    PubMed  Google Scholar 

  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.

    PubMed  Google Scholar 

  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.

    PubMed  Google Scholar 

  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.

    CAS  PubMed  Google Scholar 

  14. Kang HW, No JH, Chung JH, et al. Prevalence, clinical and ultrasonographic characteristics of thyroid incidentalomas. Thyroid. 2004;14(1):29–33.

    PubMed  Google Scholar 

  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. 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.

    PubMed  Google Scholar 

  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.

    PubMed  Google Scholar 

  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.

    PubMed  Google Scholar 

  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.

    PubMed  Google Scholar 

  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. 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.

    CAS  PubMed  Google Scholar 

  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.

    CAS  PubMed  Google Scholar 

  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.

    PubMed  Google Scholar 

  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.

    PubMed  Google Scholar 

  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. 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.

    PubMed  PubMed Central  Google Scholar 

  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.

    PubMed  Google Scholar 

  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.

    PubMed  Google Scholar 

  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.

    CAS  PubMed  Google Scholar 

  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.

    PubMed  Google Scholar 

  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.

    PubMed  Google Scholar 

  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.

    PubMed  Google Scholar 

  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. 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.

    PubMed  Google Scholar 

  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. 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.

    PubMed  PubMed Central  Google Scholar 

  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.

    PubMed  PubMed Central  Google Scholar 

  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.

    PubMed  Google Scholar 

  39. Kalantari S. The diagnostic value of color Doppler ultrasonography in predicting thyroid nodules malignancy. Int Tinnitus J. 2018;22(1):35–9.

    PubMed  Google Scholar 

  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.

    CAS  PubMed  Google Scholar 

  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. 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. 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.

    CAS  PubMed  Google Scholar 

  44. Solbiati L, Volterrani L, Rizzatto G. The thyroid gland with low uptake lesions: evaluation by ultrasound. Radiology. 1985;155(1):187–91.

    CAS  PubMed  Google Scholar 

  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. Ross DS. Nonpalpable thyroid nodules—managing an epidemic. J Clin Endocrinol Metab. 2002;87(5):1938–40.

    CAS  PubMed  Google Scholar 

  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.

    PubMed  Google Scholar 

  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.

    CAS  PubMed  Google Scholar 

  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.

    PubMed  Google Scholar 

  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.

    CAS  PubMed  Google Scholar 

  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.

    CAS  PubMed  Google Scholar 

  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.

    PubMed  Google Scholar 

  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.

    CAS  PubMed  Google Scholar 

  54. Wong KT, Ahuja AT. Ultrasound of thyroid cancer. Cancer Imaging. 2005;5(1):157–66.

    CAS  PubMed  PubMed Central  Google Scholar 

  55. Brown CL. Pathology of the cold nodule. Clin Endocrinol Metab. 1981;10(2):235–45.

    CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Mother and Child Welfare Research Center, Hormozgan University of Medical Sciences, Bandar Abbas, Iran

    L. Darvish & N. Roozbeh

  2. Department of Radiology, Faculty of Paramedicine, Hormozgan University of Medical Sciences, Bandar Abbas, Iran

    L. Darvish

  3. Hormozgan University of Medical Sciences, Bandar Abbas, Iran

    M. Khezri

  4. Paramedical School, Hormozgan University of Medical Sciences, Bandar Abbas, Iran

    S. H. Teshnizi

  5. Social Determinants of Health Research Center, Shahrekord University of Medical Sciences, Shahrekord, Iran

    J. G. Dehkordi

  6. Department of Medical Physics, Faculty of Medicine, School of Medicine, Iran University of Medical Sciences, Tehran, Iran

    A. Amraee

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  1. L. Darvish
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Darvish, L., Khezri, M., Teshnizi, S.H. et al. Color Doppler ultrasonography diagnostic value in detection of malignant nodules in cysts with pathologically proven thyroid malignancy: a systematic review and meta-analysis. Clin Transl Oncol 21, 1712–1729 (2019). https://doi.org/10.1007/s12094-019-02105-y

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