The global prevalence of thyroid cancer has increased significantly in recent years. Ultrasonography is the preferred method for differentiating benign and malignant thyroid nodules preoperatively and is recommended by guidelines.
OBJECTIVE:
To assess the application value of gray-scale ultrasound and shear wave elastography in distinguishing small thyroid nodules.
METHODS:
A retrospective analysis of 228 thyroid nodules, all of which were confirmed by pathology after surgery or FNA from January 2019 to January 2020, was carried out. All nodules were divided into a 5 mm group and a 5 mm group according to their maximum size. We compared the differences in the gray scale and elastography of the nodules between the two groups and the accuracy of different diagnostic methods.
RESULTS:
The accuracies of gray-scale ultrasound and shear wave elastography in the 5 mm group were found to be lower than those in the 5 mm group, and the gray-scale accuracy was slightly higher than that of shear wave elastography in both groups ( 0.05). The largest AUC (area under the curve) of elastic parameters in the 5 mm and 5 mm groups was found for Emax and Esd, respectively. Based on a combination of these two parameters, the accuracies of the two groups were significantly higher than those of the parameters or gray scale alone ( 0.05) and were 84.62% and 85.48%, respectively.
CONCLUSION:
Shear wave elastography is valuable in the diagnosis of benign and malignant thyroid nodules using ultrasonography. When combining gray-scale ultrasound and shear wave elastography, the diagnostic accuracy is obviously improved, especially for 5 mm small thyroid nodules.
The global prevalence of thyroid cancer has increased significantly in recent years, with papillary thyroid microcarcinoma (PTMC) being dominant, according to Surveillance, Epidemiology, and End Results (SEER) [1]. While the prognosis of PTMC is good, it may progress and have potential risk, for any papillary thyroid carcinoma (PTC) originates from cases of tiny PTMC. Furthermore, some PTMCs are high-risk pathology subtypes, prone to local invasion or lymph node metastasis [2].
Ultrasonography is the preferred method for differentiating benign and malignant thyroid nodules preoperatively and is recommended by guidelines [3] due to its high resolution and sensibility. However, some suspicious signs on ultrasound may be lag behind for the small nodules. To compensate, fine-needle aspiration (FNA) is the most accurate method [3], but it is invasive and size-limited and depends on the experience of the doctors and pathologists, under whom the cytopathology may be nondiagnostic and indeterminate. Overall, definitive diagnosis and risk classification of PTMC are difficult.
Shear wave elastography (SWE) is a new ultrasonic technique that can quantitatively analyze the hardness of nodules to aid in diagnosis. Recent clinical studies have used this technique for differential diagnosis and disease assessment, and many [4, 5, 6] have confirmed that it is particularly useful for occupying lesions in breast, prostate, and thyroid. However, there is no report on differential diagnosis using quantitative parameters of SWE for small thyroid nodules, and it is unclear whether it is advantageous or what the degree of benefit is. Therefore, in this study, we analyzed tiny thyroid nodules with gray-scale ultrasound and SWE of benign and malignant nodules and evaluated their differential diagnostic values.
Materials and methods
This study was approved by the ethics committee and review board of our hospital before reviewing patients’ clinical data. We performed our analyses in accordance with the relevant guidelines and regulations.
Patients
A retrospective case analysis of 289 thyroid nodules from 230 patients was carried out from January 2019 to January 2020. All had preoperative ultrasound and SWE examination, and all nodules were subject to pathology from FNA or surgical operation in our hospital. 174 patients (209 nodules) received FNA: 130 patients (162 nodules) of them underwent surgery, 44 patients (47 nodules) of them took follow-up and some of them had second FNA. Other 56 patients (80 nodules) went on direct operation without FNA.
Among them, 20 nodules were excluded: 13 nodules had cystic portions greater than 10% for that they may have affected the outcome of the SWE data, 7 had a history of intervention (including FNA, ablation, and sclerotherapy). For the remaining nodules, the following inclusion criteria were applied: (a) nodule diameter 10 mm and visible on ultrasound; (b) ultrasound and SWE examination were completed before FNA, and the SWE image is stable and the relevant data are complete (23 nodules were excluded); (c) clear histopathology, and the cytological pathology of FNA-Bethesda class II is also required when they were under review for six months at least or had second FNA with FNA II. Then 18 nodules of Bethesda classes III (indistinct follicular lesion or atypical lesion), IV (follicular neoplasm or suspicious for follicular neoplasm), and I (non-diagnostic) without definitive histopathological results from further FNA or surgery were subsequently excluded. Finally, 172 patients with a total of 228 nodules were included.
Gray-scale ultrasound
We used a real-time sonography (Aixplorer, SuperSonic Imagine, Aix en Provence, France) equipped with an SL15-4 linear-array probe for gray-scale ultrasound and SWE. All examinations were performed by one doctor with more than five years of experience in thyroid. Each patient was placed in a comfortable supine position, and routine transverse and longitudinal sections were fully scanned. Parameters were adjusted according to the target nodule position to clearly show details of the nodule. According to the relevant guidelines and recommendations [7, 8], the following features were recorded: nodule size, echogenicity (hyper-, iso-, hypo-, very hypo-, or mix-, in comparison with the surrounding thyroid tissue and strap muscles), morphology (A/T 1 and A/T 1, anteroposterior and transverse diameter ratios in both maximum transverse and longitudinal sections; a ratio in any section greater than one indicted the former), margin (smooth, rough), calcification (no calcification, macrocalcification 1 mm with acoustic shadow, microcalcification 1 mm without acoustic shadow, and macrocalcification mixed with microcalcification). Finally, each thyroid nodule was classified by the Thyroid Imaging Report and Data System (TI-RADS) [8].
Shear wave elastography
After stabilization in gray-scale mode, the examiner initiated SWE with an SL15-4 linear probe, kept the probe in vertical contact with the skin, and applied an appropriate coupling agent to reduce pressure. The size of the sampling frame was usually about 2 times the size of the nodule, and the whole target nodule and part of the subcutaneous tissue and surrounding thyroid tissue were included. The measuring range of Young’s modulus was 0 70 kPa. The patient was then asked to gently close his/her lips, hold his/her breath, and remain still for 3 5 s. Eligible and clear image criteria were as follows: the sampling frame was filled with color without obvious pressure artifacts front and rear. This process was repeated 5–8 times, and finally only the SWE image with the best stability and repeatability was selected for storage and measuring analysis.
Standard measuring of elastic parameters.
All nodules were quantitatively analyzed in longitudinal sections. We choose the “Q-Box trace” mode, which manually describes the boundary of nodules (as the region of interest, ROI) according to the margin of the gray-scale image (double contrast). After the first and last connections were confirmed, Young’s modulus (kPa), including the maximum value (Emax), mean value (Emean), minimum value (Emin), and standard deviation (Esd), was determined (Fig. 1). Then the “Q-Box ratio” mode was activated, and the Q-Box diameter was adjusted to 2 mm. The first Q-Box was placed at the location with the highest hardness of the nodule, and the second Q-Box was placed at the same depth of normal thyroid tissue at least 5 mm above the edge of the nodule. The system automatically calculated the hardness ratio (Fig. 1).
Statistical analysis
We used Stata/SE 14.2 and MedCalc 19.0 statistical software for analysis. Measurement data are shown as the means standard deviation, and classification data are expressed as numbers and percentages. For variables that conformed to a normal distribution and passed a variance homogeneity test, we applied two independent-sample tests or Wilcoxon rank sum tests to compare the differences in continuous variables. The chi-square test was used for differences among classification variables. We constructed receiver operating characteristic (ROC) curves, calculated the areas under the curve of each elastic parameter, and then compared the differences in AUC of each elastic parameter in the two groups. At the maximum of the Youden index (sensitivity specificity 1), the value of a continuous variable is the critical value. Finally, the McNemar chi-square test was used to compare the accuracy of the different diagnostic methods. 0.05 was taken as statistically significant.
Results
There were 172 patients, among whom there were 83 benign nodules and 145 malignant nodules. All malignant nodules were confirmed by postoperative pathology in our hospital, and all were papillary thyroid cancer. As to the 83 benign nodules, there were nodular hyperplasia in 44 (53.01%), Bethesda cytology class II (follow-up for six months) in 29 (34.94%), nodules caused by Hashimoto thyroiditis in 6 (7.23%), and follicular adenoma in 4 (4.82%), respectively.
Gray-scale ultrasonography
All nodules were divided into two groups according to the maximum diameter: 5 mm and 5 mm. The 5 mm group had 104 nodules, 43 benign and 61 malignant nodules, and the 5 mm group had 124 nodules, 40 benign and 84 malignant nodules.
TI-RADS classification in gray scale and combined diagnosis
TI-RADS
5 mm group
5 mm group
Malignant ( 61)
Benign ( 43)
Malignant ( 84)
Benign ( 40)
3
0
17
0
22
4a
16/(6)
14/(16)
19/(14)
10/(14)
4b
21/(31)
9/(7)
23/(28)
6/(2)
4c
24
3
37
2
5
0
0
5
0
“/( )” The values in parentheses are counts of classification in combined diagnosis.
According to the TI-RADS [8], the specific classification counts are shown in Table 1. In our study, regard those nodules which TI-RADS classifications were 4a or less as benign, those were 4b and above as malignant. Finally, compared with pathology, the sensitivity, specificity, accuracy, LR, and LR values of the TI-RADS classification in the 5 mm group were 73.77%, 72.09%, 73.08%, 2.64, and 0.36; in the 5 mm group, they were 77.38%, 80.00%, 78.23%, 3.87, and 0.28, respectively (Table 2).
Diagnostic values of gray-scale, SWE and combined diagnostic method
Sensitivity (%)
Specificity (%)
Accuracy (%)
LR
LR
5 mm group
Very hypo-echogenic
55.74
65.12
59.62
1.60
0.68
A/T 1
73.77
53.49
65.38
1.59
0.49
Rough margin
83.61
58.14
73.08
2.00
0.28
TI-RADS
73.77
72.09
73.08
2.64
0.36
Emax
73.77
69.77
72.12
2.44
0.38
Combined
90.16
76.74
84.62
3.88
0.13
5 mm group
Very hypo-echogenic
54.76
85.00
64.52
3.65
0.53
A/T 1
57.14
62.50
58.87
1.52
0.69
Rough margin
91.67
72.50
85.48
3.33
0.11
Microcalcification
55.95
70.00
60.48
1.87
0.63
TI-RADS
77.38
80.00
78.23
3.87
0.28
Esd
67.86
92.50
75.81
9.05
0.35
Combined
83.33
90.00
85.48
8.33
0.19
Comparison of gray-scale and elastic features in 5 mm group
Features
Malignant ( 61)
Benign ( 43)
Echogenicity (%)
0.036
Very hypo-
34 (55.7)
15 (34.9)
Hypo-
24 (39.3)
23 (53.5)
Iso-
3 (4.9)
4 (9.3)
Hyper-
0
0
Mix-
0 (0)
1 (2.3)
Morphology (%)
0.005
A/T 1
45 (73.8)
20 (46.5)
A/T 1
16 (26.2)
23 (53.5)
Margin (%)
0.000
Rough
51 (83.6)
18 (41.9)
Smooth
10 (16.4)
25 (58.1)
Calcification (%)
0.076
Microcalcification
21 (34.4)
8 (18.6)
Macrocalcification
1 (1.6)
0 (0)
Mix
1 (1.6)
0 (0)
No
38 (62.3)
35 (81.4)
Elastic parameters (kPa)
Emax
37.48 13.11
27.37 10.57
0.000
Emin
17.43 7.48
15.58 7.52
0.219
Emean
27.07 9.51
21.18 8.82
0.002
Esd
4.69 2.57
3.00 1.58
0.000
Ratio
1.86 0.66
1.48 0.58
0.000
There was a significant difference for very hypo-echogenic with other echogenicity ( 0.05); microcalcification was not significantly different with other calcification form between benign and malignant nodules ( 0.05).
Comparison of gray-scale and elastic features in the 5 mm group
Features
Malignant ( 84)
Benign ( 40)
Echogenicity (%)
0.000
Very hypo-
46 (54.8)
6 (15.0)
Hypo-
36 (42.9)
21 (52.5)
Iso-
0 (0)
0 (0)
Hyper-
0 (0)
0 (0)
Mix-
2 (2.4)
13 (32.5)
Morphology (%)
0.041
A/T 1
48 (57.1)
15 (37.5)
A/T 1
36 (42.9)
25 (62.5)
Margin (%)
0.000
Rough
77 (91.7)
11 (27.5)
Smooth
7 (8.3)
29 (72.5)
Calcification (%)
0.007
Microcalcification
47 (56.0)
12 (30.0)
Macrocalcification
1 (1.2)
1 (2.5)
Mix
6 (7.1)
1 (2.5)
No
30 (35.7)
26 (65.0)
Elastic parameters (kPa)
Emax
48.80 26.89
29.25 8.97
0.000
Emin
15.05 9.69
12.95 5.22
0.394
Emean
29.63 14.98
19.59 5.32
0.000
Esd
7.22 5.94
3.27 1.62
0.000
Ratio
2.46 1.30
1.60 0.76
0.000
There was a significant difference for very hypo-echogenic, microcalcification from other modality of echogenicity and calcification between benign and malignant nodules ( 0.05).
Echogenicity, morphology, and margin differed between benign and malignant nodules in the 5 mm group ( 0.05), However, there was no significant difference in microcalcification ( 0.05) (Table 3). Benign and malignant nodules of the 5 mm group were significantly different with respect to echogenicity, morphology, margin, and microcalcification ( 0.05) (Table 4).
In the 5 mm group, the accuracy of the rough margin was the highest (73.08%), A/T 1 was the second highest (65.38%), and the difference was statistically significant ( 0.05) (Table 3). In the 5 mm group, the highest diagnostic sensitivity and accuracy values were obtained for the rough margins of nodules, 91.67% and 85.48%, respectively, followed by very hypo-echogenic nodules (64.52%), and there was no significant difference in accuracy ( 0.05) (Table 4).
Shear wave elastography
As shown in Tables 3 and 4, in both groups, the maximum value of Young’s modulus (Emax), the mean value (Emean), the standard deviation (Esd), and the ratio of Young’s modulus to normal glands (Ratio) of malignant nodules were significantly higher than those of benign nodules ( 0.05). The minimum value (Emin) was not significantly different between benign and malignant nodules ( 0.05). According to the ROC curves, the AUC values of Emax, Esd, Ratio, and Emean in the 5 mm group were 0.723, 0.715, 0.704, and 0.679, respectively (Fig. 2), and there was no significant difference between any of these variables ( 0.05). The AUC of Emax was the largest, and at a critical value of 31.0 kPa, had the highest diagnostic accuracy, sensitivity, specificity, LR, and LR values of 73.77%, 69.77%, 72.12%, 2.44, and 0.38, respectively (Table 2).
ROC of elastic parameters in the 5 mm group.
ROC of elastic parameters in the 5 mm group.
In the 5 mm group, the AUC values of Esd, Emax, Ratio, and Emean were 0.853, 0.819, 0.784, and 0.761, respectively (Fig. 3), and there was no significant difference between the AUC of Esd and Emax ( 0.05), but there were significant differences between Esd and Emean, also between Emax and Emean ( 0.05). Esd had the largest AUC, and when the critical value was 4.8 kPa, the diagnostic performance values for sensitivity, specificity, accuracy, LR, and LR were 67.86%, 92.50%, 75.81%, 9.05, and 0.35, respectively (Table 2).
Combined diagnosis
Later, we combinate the TI-RADS classification with the best elastic parameters, for primary TI-RADS 4a nodules in the 5 mm group, when Emax 31.0 kPa, TI-RADS classification increased to 4b; for TI-RADS 4b nodules when Emax 31.0 kPa, TI-RADS was reduced to 4a. For nodules that did not meet the above criteria, the classification remained unchanged. In the 5 mm group, the best elastic parameter was Esd, the cut-off value was 4.8 kPa, and the combined diagnostic classification criteria were the same as in the 5 mm group.
The TI-RADS classification count of combined diagnosis is shown in parentheses in Table 1. The sensitivity, specificity, accuracy, LR, and LR values of the combined diagnosis in the 5 mm group were 90.16%, 76.74%, 84.62%, 3.88, and 0.13, respectively (Table 2). Accordingly, diagnosis performance of the 5 mm group in the combined diagnosis were 83.33%, 90.00%, 85.48%, 8.33, and 0.19, respectively (Table 2). The accuracy of combined diagnosis was significantly higher than that of the gray-scale ultrasound and Emax or Esd alone, and difference was statistically significant ( 0.05), and the difference between the gray-scale ultrasound and elastic parameter alone was not significantly ( 0.05).
Discussion
The new shear wave elastography aids in differential diagnosis by quantitating hardness, and some studies [6, 9] have confirmed its diagnostic value for thyroid nodules. This study explore the diagnostic value of gray-scale ultrasound and SWE imaging of micronodules, we find the accuracy of gray-scale ultrasound was slightly higher than that of shear wave elastography in both groups, and after combination of TI-RADS classification and shear wave elastography, the accuracies were significantly higher than those of the elastic parameters or gray scale alone, especially for 5 mm small thyroid nodules.
With respect to gray-scale ultrasound, there are some differences in studies of the sensitivity, specificity, and accuracy in the diagnosis of papillary thyroid microcarcinoma, with respective ranges of 91.67–97.40%, 55.10–75.71%, and 77.2–83.80% [10, 11]. In this study, we adopted the thyroid imaging report and data system (TI-RADS) proposed by Kwak et al. [8] and considered category 4b and above as malignant. The sensitivity, specificity, accuracy values of the gray-scale ultrasound for the 5 mm and 5 mm groups were 73.77%, 72.09%, 73.08% and 77.38%, 80.00%, and 78.23%, respectively. When size is unlimited and there are mainly 10 mm nodules, the diagnostic sensitivity, specificity, and accuracy values are 98.53%, 91.01%, and 92.08% and are 89.69%, 88.24%, and 89.14%, respectively, according to different reports [12, 13], which are higher than those of microcarcinoma. This shows that the diagnostic level is affected by nodule size. In this study, we also found that the accuracy in the 5 mm group (78.23%) was higher than that in the 5 mm group (73.08%).
In the 5 mm group, the following characteristics differed significantly between benign and malignant thyroid nodules, similar to previous reports [10, 11]: very hypo-echogenic, A/T 1, rough margin, and microcalcification. In the 5 mm group, only the difference in microcalcification was not significant ( 0.05). The reason may be that the incidence of microcalcification in 5 mm nodules is low, as microcalcification is associated with ischemic necrosis, vitreous degeneration, and secondary calcium deposition in tumor cells; microcarcinoma ( 5 mm) is less likely to have necrosis at such a small size. In addition, some concentrated colloids occur in benign small nodules, and strong echogenicity can also cause misdiagnosis. It has been reported that microcalcification is the best predictor of malignancy, with the highest sum of sensitivity and specificity, and the accuracy range is 76.60–81.47% [13, 14]. The highest accuracy and sensitivity in both groups in this study were obtained for rough margins, and the accuracy was 73.08% and 85.48%, respectively. Ha et al. found that when the subjects were only 5 mm or 10 mm nodules, very hypo-echogenic nodules had the highest accuracy (76.90%, 75.70%), followed by rough margin or lobular nodules (65.40%, 72.00%) [15]. Therefore, we can’t recognize only by one sign, we should pay attention to all these suspicious characteristics in gray scale when differentiating PTMCs, even more information such as elastic parameters.
The values of the elastic parameters Emax, Emean, Esd, and the Ratio of malignant nodules were significantly higher than those of benign nodules ( 0.05). That is to say, the hardness of malignant nodules was significantly higher. In our study, Emax and Esd were the best elastic indexes among all elastic parameters, similar to the reported literature for thyroid nodules of different sizes [13, 16, 17, 18, 19, 20, 21]. There are some reports that Emean is the most valuable index [22, 23, 24, 25], but the accuracy of Emean in this study was relatively low. We speculate that the differences are due to distinct measurements of the elastic parameters of the lesions, such the size and location of the ROI. Emean reflects the average of the overall hardness of nodules in our study, while Liu et al. [22] and Bhatia et al. [23] fixed the diameter of ROI to 2 mm and located it on the hardest part of the nodule, which increased the average hardness. The Emean values of benign nodules in both of the above-mentioned studies were 22.6 26.2 kPa, and those of malignant nodules were 35.6 43.1 kPa, which are higher than those obtained in our study, probably because of higher precompression that the larger nodules might be subjected to [23]. There is as yet no report on differential diagnosis using quantitative parameters of SWE for 5 mm and 5 mm, or 10 mm nodules, and study which real-time elastography (RTE) and acoustic radiation force impulse (ARFI) was adjunctive to TI-RADS for differentiating such small nodules had been published [26, 27].
A case of 5 mm PTMC in a 32-year-old woman. A, B. Gray-scale ultrasonography of transverse and longitudinal shows a diameter 5 mm nodule at the left lobe of thyroid, very-hypoechoic, A/T 1, smooth margin, no calcification, gray-scale classification of TI-RADS was 4a. C, D. SWE shows the maximum value of Young’s modulus of nodules is 48.2 kPa (Emax), Esd is 5.0 kPa. Combined diagnosis was upgraded to 4b because of its Emax 31.0 kPa; preoperative FNA classified as V grade (some abnormal follicular epithelial cells), finally, it was confirmed by paraffin section.
A case of 5 mm PTMC in a 62-year-old woman. A, B. Gray-scale ultrasonography of transverse and longitudinal shows a diameter 5 mm nodule at the right lobe of thyroid, very-hypoechoic, A/T 1, rough margin(lobulated), scattered microcalcification, gray-scale classification of TI-RADS was 4b. C, D. SWE shows the texture of the nodule is soft on the transverse and longitudinal sections, and the value of Esd is 3.5 kPa, Emax is 22.7 kPa. Combined diagnosis was downgraded to 4a for Esd 4.8 kPa. The preoperative FNA was classified as Bethesda II grade, and postoperative paraffin pathology was fibrosis nodule with inflammatory, and the surrounding thyroid tissue showed chronic lymphocytic thyroiditis.
In this study, the diagnostic accuracy of SWE alone for the two groups was lower than that of gray-scale ultrasound, but the difference was not significant ( 0.05). However, we found that the accuracy of the combined diagnosis increased significantly ( 0.05). We also observed that the accuracies of TI-RADS classification alone and SWE in the 5 mm group were lower than those of the 5 mm group, but in the combined diagnosis, the accuracies were similar finally. Therefore, combined diagnostic techniques can provide more differential diagnosis information (Figs 4 and 5), especially for 5 mm nodules. For these nodules, there are many difficulties or low rate of success for FNA. Furthermore, we also found that the sensitivity of combined diagnosis in the 5 mm group reached 90.16%. High sensitivity is helpful for the early identification of thyroid microcarcinoma and the initial screening of high-risk nodules and can effectively reduce the rate of invasive operations and failure. When nodules were 5 mm, the specificity of combined diagnosis was relatively high (90.00%), which could help to diagnose high-risk thyroid nodules accurately and provide time for FNA and surgical treatment advice. As for rate of unnecessary biopsy, a multicenter study [28] also found it decreased significantly when 2017 American College of Radiology (ACR) guidelines were combined with 3 modes of elastography (stress elastography, point shear wave elastography (pSWE), ARFI), although the nodules smaller than 10 mm were not recommended.
The limitations of this study include the following: (1) this study is a single-center study with a small sample size that may have been prone to selection bias because only papillary thyroid carcinoma and no other pathological types were found in malignant nodules. The elastic parameters of different types of thyroid carcinoma may be different. (2) The results of the elastic parameters in this study were all from longitudinal sections, but the measurement results of longitudinal sections and transverse sections of some nodules may be different; this will require additional study.
Conclusion
Both gray-scale ultrasound and SWE have diagnostic ability to differentiate thyroid micronodules ( 10 mm). A combination of the two approaches can significantly improve the diagnostic accuracy, especially for 5 mm nodules. Therefore, in addition to gray-scale ultrasound, the application of shear wave elastography is also worthwhile.
Footnotes
Conflict of interest
None to report.
References
1.
ChenWZhengRBaadePDZhangSZengHBrayF, et al. Cancer Statistics in China, 2015. CA Cancer J Clin.2016; 66: 115-132.
HaugenBRAlexanderEKBibleKCDohertyGMMandelSJNikiforovYE, et al. 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.2016; 26(1): 1-133.
4.
YoukJHGweonHMSonEJ. Shear-wave elastography in breast ultrasonography: The state of the art. Ultrasonography.2017; 36(4): 300-309.
5.
GandhiJZaidiSShahJJoshiGKhanSA. The evolving role of shear wave elastography in the diagnosis and treatment of prostate cancer. Ultrasound Q.2018; 34(4): 245-249.
6.
KimHJKwakMKChoiIHJinSParkHKByunDW, et al. Utility of shear wave elastography to detect papillary thyroid carcinoma in thyroid nodules: Efficacy of the standard deviation elasticity. Korean J Intern Med.2019; 34(4): 850-857.
7.
TesslerFNMiddletonWDGrantEGHoangJKBerlandLLTeefeySA, et al. ACR Thyroid Imaging, Reporting and Data System (TI-RADS): White Paper of the ACR TI-RADS Committee. J AM Coll Radiol.2017; 14(5): 587-595.
8.
KwakJYHanKHYoonJHMoonHJSonEJParkSH, et al. Thyroid imaging reporting and data system for US features of nodules: A step in establishing better stratification of cancer risk. Radiology.2011; 260(3): 892-899.
9.
ZhaoCKXuHX. Ultrasound elastography of the thyroid: Principles and current status. Ultrasonography.2019; 38(2): 106-124.
10.
DuYRJiCLWuYGuXG. Combination of ultrasound elastography with TI-RADS in the diagnosis of small thyroid nodules (⩽ 10 mm): A new method to increase the diagnostic performance. Eur J Radiol.2018; 109: 33-40.
11.
SchenkeSKlettRSeifertPKreisslMCGorgesRZimnyM. Diagnostic Performance of Different Thyroid Imaging Reporting and Data Systems (Kwak-TIRADS, EU-TIRADS and ACR TI-RADS) for Risk Stratification of Small Thyroid Nodules (⩽ 10 mm). J Clin Med.2020; 9(1): 236.
12.
BashaMAAAlnaggarAARefaatREi-MaghrabyAMRefaatMMElhamedMEA, et al. The validity and reproducibility of the thyroid imaging reporting and data system (TI-RADS) in categorization of thyroid nodules: Multicentre prospective study. Eur J Radiol.2019; 117: 184-192.
13.
LiuZJingHHanXShaoHSunYXWangQC, et al. Shear wave elastography combined with the thyroid imaging reporting and data system for malignancy risk stratification in thyroid nodules. Oncotarget.2017; 8(26): 43406-43416.
14.
LiuBXXieXYLiangJYZhengYLHuangGLZhouLY, et al. Shear wave elastography versus real-time elastography on evaluation thyroid nodules: A preliminary study. Eur J Radiol.2014; 83(7): 1135-1143.
15.
HaSMKimJKBaekJH. Detection of Malignancy Among Suspicious Thyroid Nodules < 1 cm on Ultrasound with Various Thyroid Image Reporting and Data Systems. Thyroid.2017; 27(10): 1307-1315.
16.
KimHJKwakMKChoiIHJinSYParkHKByunDW, et al. Utility of shear wave elastography to detect papillary thyroid carcinoma in thyroid nodules: Efficacy of the standard deviation elasticity. Korean J Intern Med.2019; 34(4): 850-857.
17.
ShangHWuBLiuZLiuYChengW, et al. The effectiveness of shear wave elastography in the diagnosis of PTMC. Technol Health Care.2020; 28(2): 221-226.
18.
VeyrieresJBAlbarelFLombardJVBerbisJSebagFOliverC, et al. A threshold value in Shear Wave elastography to rule out malignant thyroid nodules: A reality? Eur J Radiol.2012; 81(12): 3965-3972.
19.
Szczepanek-ParulskaEWolinskiKStangierskiAGurgulEBiczyskoMMajewskiP, et al. Comparison of diagnostic value of conventional ultrasonography and shear wave elastography in the prediction of thyroid lesions malignancy. PLoS One.2013; 8(11): e81532.
20.
Dobruch-SobczakKZalewskaEBGuminskaASlapaRZMlosekKWarelukP, et al. Diagnostic Performance of Shear Wave Elastography Parameters Alone and in Combination with Conventional B-Mode Ultrasound Parameters for the Characterization of Thyroid Nodules: A Prospective, Dual-Center Study. Ultrasound Med Biol.2016; 42(12): 2803-2811.
21.
ParkAYSonEJHanKYoukJYKimJAParkCS. Shear wave elastography of thyroid nodules for the prediction of malignancy in a large scale study. Eur J Radi.2015; 84(3): 407-412.
22.
LiuBLiangJZhengYXieXHuangGZhouL, et al. Two-dimensional shear wave elastography as promising diagnostic tool for predicting malignant thyroid nodules: A prospective single-centre experience. Eur Radiol.2015; 25(3): 624-634.
23.
BhatiaKSSTongCSLChoCCMYuenEHYLeeYYPAhujaAT. Shear wave elastography of thyroid nodules in routine clinical practice: Preliminary observations and utility for detecting malignancy. Eur Radiol.2012; 22(11): 2397-2406.
24.
DuanSBYuJLiXHanZYZhaiHYLiangP. Diagnostic value of two-dimensional shear wave elastography in papillary thyroid microcarcinoma. Onco Targets Ther.2016; 9: 1311-1317.
25.
LuoJChenJSunYXuFWuLHuangP. A retrospective study of reducing unnecessary thyroid biopsy for American College of Radiology Thyroid Imaging Reporting and Data Systems 4 assessment through applying shear wave elastography. Arch Endocrinol Metab.2020 Aug; 64(4): 349-355.
26.
PeiSZhangBCongSLiuJWuSDongYZhangLZhangS. Ultrasound Real-Time Tissue Elastography Improves the Diagnostic Performance of the ACR Thyroid Imaging Reporting and Data System in Differentiating Malignant from Benign Thyroid Nodules: A Summary of 1525 Thyroid Nodules. Int J Endocrinol.2020 Apr 14; 2020: 1749351.
27.
WangJWeiWGuoR. Ultrasonic elastography and conventional ultrasound in the diagnosis of thyroid micro-nodules. Pak J Med Sci.2019 Nov-Dec; 35(6): 1526-1531.
28.
WangHXLuFXuXHZhouPDuLYZhangYDingSSShiHWangDXuHXZhangYF. Diagnostic Performance Evaluation of Practice Guidelines, Elastography and Their Combined Results for Thyroid Nodules: A Multicenter Study. Ultrasound Med Biol.2020 Aug; 46(8): 1916-1927.
