Analysis of vascularization in thyroid gland nodes with superb microvascular imaging (SMI) and CD34 expression histology: a pilot study

Background The Doppler sonography technique known as "superb microvascular imaging" (SMI) is advancing sonographic micro vascularization imaging in various disciplines. In this study, we aimed to determine whether SMI could reliably reproduce the blood flow in thyroid nodes and whether malignancy could be diagnosed, based on vascularization properties. Immunhistochemical staining by CD34 and SMI where used to determine the vascularization of nodes in terms of quantified vascularization parameters gained by computational evaluation. Methods We used image analysis programs to investigate whether the quantitative value for vascularization strength in the thyroid node, measured with SMI, was correlated with the actual degree of vascularization, determined microscopically. We included 16 patients that underwent thyroid resections. We prepared thyroid gland tissue slices for immunohistochemistry and labelled endothelial cells with CD34 to visualize blood vessels microscopically. We used image analysis programs, ImageJ, to quantify SMI Doppler sonographic measurements and CellProfiler to quantify CD34 expression in histological sections. We evaluated the numeric values for diagnostic value in node differentiation. Furthermore, we compared these values to check for correlations. Results Among the 16 nodes studied, three harboured malignant tumours (18.75%): two papillary and one follicular carcinoma. Among the 13 benign lesions (81.25%), four harboured follicular adenomas. Malignant and benign nodes were not significantly different in sonographic (0.88 ± 0.89 vs. 1.13 ± 0.19; p  = 0.2790) or immunohistochemical measurements of vascularization strength (0.05 ± 0.05 vs. 0.08 ± 0.06; p  = 0.2260). Conclusion We found a positive, significant correlation (r = 0.55588; p  = 0.0254) between SMI (quantitative values for vascularization strength) and immunohistochemistry (CD34 staining) evaluations of thyroid nodes.

[1]  Gilles Russ,et al.  Prospective evaluation of thyroid imaging reporting and data system on 4550 nodules with and without elastography. , 2013, European journal of endocrinology.

[2]  R. Paschke,et al.  Comparison of Color Flow Doppler Sonography (CFDS) and immunohistologic detection of microvessels for the assessment of the malignancy of thyroid nodules. , 2010, Hormone and metabolic research = Hormon- und Stoffwechselforschung = Hormones et metabolisme.

[3]  R. Paschke,et al.  2013 European Thyroid Association Guidelines for Cervical Ultrasound Scan and Ultrasound-Guided Techniques in the Postoperative Management of Patients with Thyroid Cancer , 2013, European Thyroid Journal.

[4]  Correlation of contrast-enhanced ultrasonographic features with microvessel density in papillary thyroid carcinomas. , 2014, Asian Pacific journal of cancer prevention : APJCP.

[5]  Xun Wang,et al.  Superb microvascular imaging (SMI) compared with conventional ultrasound for evaluating thyroid nodules , 2017, BMC Medical Imaging.

[6]  J. Bojunga.  Ultrasound of Thyroid Nodules , 2018, Ultraschall in der Medizin - European Journal of Ultrasound.

[7]  A. Lyshchik,et al.  Microvascular blood flow in the thyroid: Preliminary results with a novel imaging technique , 2014, 2014 IEEE International Ultrasonics Symposium.

[8]  Yi-Cheng Zhu,et al.  A Prospective Study to Compare Superb Microvascular Imaging with Grayscale Ultrasound and Color Doppler Flow Imaging of Vascular Distribution and Morphology in Thyroid Nodules , 2018, Medical science monitor : international medical journal of experimental and clinical research.

[9]  Jia Zhan,et al.  Superb Microvascular Imaging-A new vascular detecting ultrasonographic technique for avascular breast masses: A preliminary study. , 2016, European journal of radiology.

[10]  A. Fleischer,et al.  Sonographic Quantification of Ovarian Tumor Vascularity , 2006, Journal of ultrasound in medicine : official journal of the American Institute of Ultrasound in Medicine.

[11]  N. Arsenijević,et al.  Angiogenic and lymphangiogenic profiles in histological variants of papillary thyroid carcinoma. , 2017, Polish archives of internal medicine.

[12]  Argon Chen,et al.  Quantitative analysis of dynamic power Doppler sonograms for patients with thyroid nodules. , 2013, Ultrasound in Medicine and Biology.

[13]  Hyun Joo Shin,et al.  Superb microvascular imaging for the detection of parenchymal perfusion in normal and undescended testes in young children. , 2016, European journal of radiology.

[14]  E. Horvath,et al.  Prospective validation of the ultrasound based TIRADS (Thyroid Imaging Reporting And Data System) classification: results in surgically resected thyroid nodules , 2017, European Radiology.

[15]  Tamotsu Kamishima,et al.  Power Doppler signal calibration in the finger joint between two models of ultrasound machine: a pilot study using a phantom and joints in patients with rheumatoid arthritis , 2017, Acta radiologica.

[16]  angesichts der Corona-Pandemie,et al.  UPDATE , 1973, The Lancet.

[17]  Rui-Na Zhao,et al.  Role of Superb Micro‐Vascular Imaging in the Preoperative Evaluation of Thyroid Nodules: Comparison With Power Doppler Flow Imaging , 2017, Journal of ultrasound in medicine : official journal of the American Institute of Ultrasound in Medicine.

[18]  T. Stout,et al.  Relationship between colour flow Doppler sonographic assessment of corpus luteum activity and progesterone concentrations in mares after embryo transfer. , 2016, Animal reproduction science.

[19]  J. Wass,et al.  Angiogenesis and lymphangiogenesis in thyroid proliferative lesions: relationship to type and tumour behaviour. , 2004, Endocrine-related cancer.

[20]  Neil Blumberg,et al.  Tumor Angiogenesis Factor , 1974, The Yale journal of biology and medicine.

[21]  A. Lyshchik,et al.  A Novel Microvascular Flow Technique: Initial Results in Thyroids , 2016, Ultrasound quarterly.

[22]  Yue Chen,et al.  Additional Value of Superb Microvascular Imaging for Thyroid Nodule Classification with the Thyroid Imaging Reporting and Data System. , 2019, Ultrasound in medicine & biology.

[23]  Yongfeng Zhao,et al.  Application of a Novel Microvascular Imaging Technique in Breast Lesion Evaluation. , 2016, Ultrasound in medicine & biology.

[24]  J. Shin,et al.  The Diagnostic Performance of Thyroid US in Each Category of the Bethesda System for Reporting Thyroid Cytopathology , 2016, PloS one.

[25]  Comparison of color-Doppler and qualitative and quantitative strain-elastography for differentiation of thyroid nodules in daily practice , 2016, Hormones.

[26]  Grace C H Yang,et al.  Most Thyroid Cancers Detected by Sonography Lack Intranodular Vascularity on Color Doppler Imaging: Review of the Literature and Sonographic‐Pathologic Correlations for 698 Thyroid Neoplasms , 2017, Journal of ultrasound in medicine : official journal of the American Institute of Ultrasound in Medicine.

[27]  Paolo Vitti,et al.  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. , 2016, Endocrine practice : official journal of the American College of Endocrinology and the American Association of Clinical Endocrinologists.

[28]  Jue Jiang,et al.  Correlation Between Maximum Intensity and Microvessel Density for Differentiation of Malignant From Benign Thyroid Nodules on Contrast‐Enhanced Sonography , 2014, Journal of ultrasound in medicine : official journal of the American Institute of Ultrasound in Medicine.

[29]  M. Kendall,et al.  Measurement of vascularity as a diagnostic and prognostic tool for well differentiated thyroid tumours: comparison of different methods of assessing vascularity. , 1999, Journal of clinical pathology.

[30]  M. Castellano,et al.  Ultrasound Microvascular Blood Flow Evaluation: A New Tool for the Management of Thyroid Nodule? , 2019, International journal of endocrinology.

[31]  B. Choi,et al.  Distinguishing benign from malignant thyroid nodules using thyroid ultrasonography: utility of adding superb microvascular imaging and elastography , 2018, La radiologia medica.

[32]  J. Szejnfeld,et al.  Flow Pattern and Vascular Resistive Index as Predictors of Malignancy Risk in Thyroid Follicular Neoplasms , 2005, Journal of ultrasound in medicine : official journal of the American Institute of Ultrasound in Medicine.

[33]  Jae Young Lee,et al.  Superb microvascular imaging technology for ultrasound examinations: Initial experiences for hepatic tumors. , 2016, European journal of radiology.

[34]  Min Jung Kim,et al.  Thyroid Imaging Reporting and Data System and Ultrasound Elastography: Diagnostic Accuracy as a Tool in Recommending Repeat Fine-Needle Aspiration for Solid Thyroid Nodules with Non-Diagnostic Fine-Needle Aspiration Cytology. , 2016, Ultrasound in medicine & biology.

[35]  Hilde van der Togt,et al.  Publisher's Note , 2003, J. Netw. Comput. Appl..

[36]  Kyunghwa Han,et al.  Can increased tumoral vascularity be a quantitative predicting factor of lymph node metastasis in papillary thyroid microcarcinoma? , 2014, Endocrine.

[37]  Gilles Russ,et al.  Risk stratification of thyroid nodules on ultrasonography with the French TI-RADS: description and reflections , 2015, Ultrasonography.

[38]  Jin Young Kwak,et al.  Can vascularity at power Doppler US help predict thyroid malignancy? , 2010, Radiology.

[39]  M. Ringel,et al.  Thyroid nodules and cancer management guidelines: comparisons and controversies. , 2017, Endocrine-related cancer.

[40]  T. Desser,et al.  Ultrasound of thyroid nodules. , 2008, Neuroimaging clinics of North America.

[41]  E. Kandil,et al.  Is vascular flow a predictor of malignant thyroid nodules? A meta-analysis. , 2016, Gland surgery.

[42]  H. Moon,et al.  Application of Various Additional Imaging Techniques for Thyroid Ultrasound: Direct Comparison of Combined Various Elastography and Doppler Parameters to Gray-Scale Ultrasound in Differential Diagnosis of Thyroid Nodules. , 2018, Ultrasound in medicine & biology.