Clinical Imaging xxx (2013) xxx–xxx

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Original Research

The value of ultrasound elastography in differentiation of malignancy in thyroid nodules Mehmet Arif Akcay a, Aslihan Semiz-Oysu b,⁎, Rengin Ahiskali c, Erkin Aribal d a

Department of Radiology, Sanliurfa Children’s Hospital, Sanliurfa, Turkey Department of Radiology, Umraniye Training and Research Hospital, Istanbul, Turkey Department of Pathology, Marmara University Hospital, Istanbul, Turkey d Department of Radiology, Marmara University Hospital, Istanbul, Turkey b c

a r t i c l e

i n f o

Article history: Received 10 July 2013 Received in revised form 12 October 2013 Accepted 14 November 2013 Available online xxxx Keywords: Elastography Fine needle aspiration biopsy Nodule Thyroid gland Ultrasound

a b s t r a c t We aimed to determine the value of ultrasound elastography (US-E) using carotid artery pulsation in differentiation of malignant and benign thyroid nodules. One hundred ten nodules were evaluated by US-E, and stiffness scores were compared to biopsy results. When cutoff for malignancy was determined as score 4, sensitivity, specificity, positive predictive value, and negative predictive value were 100%, 95%, 40%, and 100%, respectively. We suggest fine needle aspiration biopsy to be performed in all score 4 nodules, while biopsy may be unnecessary in score 1 nodules. Benign biopsy result in a score 4 nodule should suggest radiological– pathological disagreement, and repeat biopsy should be recommended. © 2013 Elsevier Inc. All rights reserved.

1. Introduction Thyroid gland nodules are common, and palpable nodules are found in between 4% and 7% of the adult population [1,2]. Widespread use of ultrasound (US) imaging and development of high-resolution scanners have significantly improved the detection of thyroid nodules [2]. According to US imaging and autopsy results, the incidence of thyroid nodules may increase up to 50% of population [3–5]. The rate of malignancy among thyroid nodules range between 5% and 15% [6,7]. US imaging is a definitive method for detection of thyroid nodules; however, the predictive value of US in differentiation of malignant nodules is limited [8,9]. Currently, the best available method for discrimination of malignant from benign thyroid nodules is fine needle aspiration biopsy (FNAB) [10–12]. Despite its high sensitivity and specificity, FNAB is an invasive procedure and may give nondiagnostic results in 10% to 20% of biopsies [6]. Palpation is clinically used to evaluate the stiffness of a thyroid nodule; however, it is a subjective method, and findings depend on the size and location of the nodule as well as the examiner’s skill [13]. Elastography is a recently introduced noninvasive technique which estimates the stiffness of tissues by assessing distortion under compression [14,15]. US elastography has been successfully applied in the breast and more recently in the prostate gland [16]. Previous ex

vivo and in vivo studies have documented significant differences in stiffness of normal thyroid tissue and tumors of the thyroid gland [17,18]. However, out-of-plane motion of the nodule during external compression and compression of the thyroid gland due to pulsation of the carotid artery may limit this technique [17]. Carotid pulsation has also been used as a source of compression for elastography of the thyroid gland [19,20]. In this study, we aimed to determine the diagnostic value of US elastography in the differentiation of malignant and benign thyroid nodules using carotid artery pulsation as the source of compression. 2. Materials and methods 2.1. Patients The study protocol was approved by the institutional ethical committee, and informed consent was obtained from the patients. The patients who were diagnosed with a thyroid nodule and had an indication for an FNAB were included into the study. The patients were selected prospectively and consecutively. The patients who did not have a final histopathological or cytological diagnosis were excluded from the study. 2.2. Lesion evaluation

⁎ Corresponding author. Umraniye Egitim ve Arastirma Hastanesi, Radyoloji Klinigi, Adem Yavuz Cad. No: 1, 34766 Umraniye, Istanbul, Turkey. Tel.: +90 216 6321818; fax: +90 216 6327121. E-mail address: [email protected] (A. Semiz-Oysu).

US elastography examinations were performed using a 5–13-MHz linear transducer (Acuson Antares, Siemens, Erlangen, Germany). All examinations were performed by the first radiologist. Baseline US

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Please cite this article as: Akcay MA, et al, The value of ultrasound elastography in differentiation of malignancy in thyroid nodules, Clin Imaging (2013), http://dx.doi.org/10.1016/j.clinimag.2013.11.008

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M.A. Akcay et al. / Clinical Imaging xxx (2013) xxx–xxx

data were collected from these studies, and related strain images were recorded in the US system as static images and also as short videos. Two radiologists evaluated the images separately and blinded. The first radiologist scored the lesions during real-time examination. Dynamic US elastographic evaluation by the first radiologist took approximately 5–10 min. The second radiologist scored the lesions on the recorded video clips separately from the first radiologist. Elastography was performed by freehand technique, and carotid pulsation was used to obtain elastography images. A rectangular region of interest was positioned to examine the targeted nodule. Images were displayed in a split screen mode where grayscale images were positioned on the right and the translucent color scale elastography images were shown superimposed on B-mode images. The color scale ranged from red showing the stiffness of the tissue to blue showing the softness. Elastography images were classified according to the scores defined by Asteria et al. [20]. This elasticity scoring originated from the elastography by Itoh et al. [21] which classifies the elastography scores on a scale of 1 to 4. Score 1 indicated elasticity in the whole nodule, score 2 elasticity in a large part of the nodule, score 3 elasticity in a small part of the nodule, and score 4 no elasticity in the nodule [20]. 2.3. Histopathological diagnosis After performing US elastography, US-guided FNAB was performed. The patient’s neck was extended by placing a pillow under the shoulder [22]. The skin was sterilized using iodine solution followed by an alcohol swipe. Local anesthesia was not routinely used. Aspiration was performed manually using a 22-gauge needle attached to a 10-cc syringe. The needle was advanced into the nodule under US guidance. Then, the needle was moved to and fro inside the nodule by applying suction and removed from the nodule. The material was handled by the pathologist present on site for preliminary cytological analysis. The procedure was repeated until sufficient material for diagnosis was obtained or up to five needle punctures. Cytological results were divided into three groups for statistical evaluation: benign, malignant, and insufficient material. Patients with insufficient cytological results underwent repeat biopsy in 3 months after the first procedure. The patients who had an insufficient result for the second time were excluded from the study. The patients who were diagnosed with FNAB as malignant, suspicious, or follicular adenoma underwent thyroidectomy. The histopathological findings of these patients were accepted as gold standard. Patients who were not operated and with FNAB results suspicious for malignancy or insufficient material were excluded from the study. All nodules that were diagnosed benign with FNAB were accepted as benign. 2.4. Statistical analysis χ 2 test was performed in order to compare the strain scores between benign and malignant nodules. In order to determine the diagnostic accuracy of US elastography for the first and second radiologists compared to histopathological or cytological results, cross-table tests were performed. Sensitivity, specificity, positive predictive value (PPV), and negative predictive value (NPV) were calculated. Kappa coefficient was used to test the interobserver concordance.

analyzed in the study. The mean age of the patients was 52.8± 12.5 years (ranging between 24 and 84 years). FNAB was performed on two nodules in eight patients, three nodules in one patient, and solitary nodules in the remaining patients. The longest dimension of the nodules ranged between 4.2 mm and 45 mm (mean 19.88± 9.4 mm). Cytological results were benign in 93 (90.3%) and malignant in 10 (9.7%) nodules. Histopathological examination revealed 6 papillary carcinomas, 3 follicular carcinomas, and 1 anaplastic carcinoma among the 10 malignant nodules. US elasticity scores and histopathological or cytological results are summarized in Table 1. All lesions scored 1 by the first radiologist and the second radiologist were diagnosed to be benign by cytology. All four score 4 lesions by the first radiologist, while three of score 4 lesions of the second radiologist, were malignant. Diagnostic accuracy of US elastography in differentiation of malignant and benign nodules was tested at different cutoff levels according to elastographic scores (Table 2). According to the first radiologist’s classification, when nodules with an elasticity score of 1, 2, and 3 were accepted benign and score 4 was accepted malignant, US elastography showed a sensitivity, specificity, PPV, and NPV of 100%, 93%, 40%, and 100%, respectively. The distribution of malignant nodules according to their elastography scores was summarized in Table 3. Three papillary carcinomas were given a score of 4 by both radiologists. One nodule with papillary carcinoma was score 2 and another papillary carcinoma was score 3 in the first and second radiologists’ classifications. One papillary carcinoma was given a score of 4 by the first radiologist and 3 by the second radiologist. One nodule with anaplastic carcinoma had a score of 2 by the first and second radiologists, separately. One nodule with follicular carcinoma was given a score of 3 by the first radiologist and a score of 2 by the second radiologist. The remaining two nodules with follicular carcinoma had a score of 3 by the first and second radiologists, separately. Statistically significant correlation was found among the first radiologist’s assessment and the second radiologist’s assessment (Pb .001) (Table 4). Moderate concordance was present between the first and the second radiologist’s assessments (kappa: 0.51). 4. Discussion Advances in imaging techniques have increased the number of documented thyroid nodules considerably; however, characterization of the lesion accurately is not always possible [23,24]. In determination of the malignant lesion, presence of microcalcifications, irregular margins, and intranodular (type III) vascularization are reported to have a high specificity but low sensitivity [25,26]. Despite its advantages, US-guided FNAB is an invasive procedure which may cause sampling errors, especially in hemorrhagic lesions, multinodular goiter, and extreme nodule sizes (smaller than 1 cm or larger than 4 cm). In cytological examination, diagnosis depends predominantly on nuclear features, which are usually unreliable predictors of the malignant potential of endocrine cells [27]. False-negative results

Table 1 US elasticity scores and histopathological and/or cytological results of the nodules

3. Results A total of 110 thyroid nodules of 99 patients were included in the study. Five nodules from five patients were excluded from the study because of insufficient material as the final cytological result. Two nodules from one patient were also excluded because the patient was lost after a diagnosis of suspicious findings for malignancy with FNAB. A total of 103 nodules from 93 patients (24 men, 69 women) were

First radiologist Benign Malignant Total Second radiologist Benign Malignant Total

Score 1

Score 2

Score 3

Score 4

Total

27 0 27

44 1 45

22 5 27

0 4 4

93 10 103

18 0 18

42 2 44

30 6 36

3 2 5

93 10 103

Please cite this article as: Akcay MA, et al, The value of ultrasound elastography in differentiation of malignancy in thyroid nodules, Clin Imaging (2013), http://dx.doi.org/10.1016/j.clinimag.2013.11.008

M.A. Akcay et al. / Clinical Imaging xxx (2013) xxx–xxx Table 2 Diagnostic accuracy of US elastography in differentiation of malignancy at different cutoff levels Assessment First radiologist First radiologist

Elasticity score 3 or 4 4

Sensitivity (%) 29 100

Specificity (%) 98 93

PPV (%) 90 40

3

Table 4 Elasticity scores given by the two radiologists Fırst radıologıst

NPV (%) 76 100

of FNAB range between 1% and 11% [10]. Moreover, up to 15%–20% of the FNABs result in an insufficient or nondiagnostic cytology [28]. US elastography is a recently introduced modality to determine the tissue stiffness and strain information noninvasively [16,29]. US elastography allows objective determination of tissue stiffness by depending on the principle that softer parts of the tissues deform easier than harder parts [30,31]. Elasticity scoring system, proposed by Itoh and Ueno, was established for the evaluation of breast lesions [22]. US elastography is reported to be useful in differentiation of the benign and malignant lesions of the prostate, breast, pancreas, and lymph nodes [16,18,32–34]. In the last years, important studies have been conducted in the differential diagnosis of thyroid nodules by US elastography [17–20,35–37]. US elastography is suggested as the best available noninvasive tool, comparable to FNAB, for the evaluation of thyroid nodules [38]. A recent meta-analysis has revealed that US elastography is a useful technique in conjunction or even instead of FNAB to select nodules for surgery [39]. Various scoring systems were used for US elastography with high sensitivity (87%–100%) and specificity (77%–100%) [17–19,35–37,40]. These scoring systems used usually consisted of 4 or 5 grades in which usually score 4 or 5 lesions were attributed to malignancy. In the current study, also a 4-grade scoring system was used [21]. Entirely elastic nodule pattern at US elastography was reported to be observed only in benign nodules [41]. According to our results, none of the score 1 lesions were diagnosed to be malignant at biopsy; therefore, we also believe that score 1 lesions may be accepted as benign and FNAB may be unnecessary in such nodules. However, score 4 lesions have a higher suspicion index of malignancy. In our series, all score 4 nodules by the first radiologist were found to be malignant, while 3 of 5 nodules (60 %) by the second radiologist were malignant. Therefore, we believe that FNAB should be performed in all nodules that display score 4 characteristics at elastography. In such patients, even if FNAB results do not propose malignancy, this may be regarded as radiological and cytological disagreement, and repeat biopsy may be recommended. Elastograpy is equivocal, however, for recommendation of biopsy in score 2 and 3 lesions. In our series, according to first radiologist’s assessment, score 2 lesions displayed a 4% malignancy, while score 3 lesions showed a 15% malignancy. Therefore, although score 3 lesions may have an increased risk of malignancy, whether FNAB should be performed for score 2 and 3

Table 3 The distribution of malignant nodules according to their elastography scores No.

Histopathological diagnosis

First radiologist's assessment

Second radiologist's assessment

1 2 3 4 5 6 7 8 9 10

Papillary carcinoma Papillary carcinoma Papillary carcinoma Papillary carcinoma Papillary carcinoma Papillary carcinoma Follicular carcinoma Follicular carcinoma Follicular carcinoma Anaplastic carcinoma

4 4 4 4 2 3 3 3 3 2

3 4 4 4 2 3 2 3 3 2

Second radiologıst

Score Score Score Score Total

1 2 3 4

Score 1

Score 2

Score 3

Score 4

Total

15 10 2 0 27

3 31 11 0 45

0 3 21 3 27

0 0 2 2 4

18 44 36 5 103

lesions should be evaluated clinically and radiologically in terms of each patient. Similar to our results, Rago et al., in their study where they have looked for the usefulness of US elastography in indeterminate or insufficient thyroid FNABs, report that softer lesions with lower scores are less likely to miss malignant lesions [42]. Stiffness of papillary carcinoma and other lesions may differ significantly [19,20]. In our series, we noted that nodules with papillary carcinoma demonstrated decreased elasticity and increased stiffness. Despite this feature of papillary carcinoma, follicular carcinoma seems to demonstrate less stiff elastographic features, similar to benign nodules [17,43]. In the current study, all three nodules diagnosed as follicular carcinoma were given a score of 2 or 3. Also, the only anaplastic carcinoma of our series was also scored 2 by both radiologists. Elastographic scoring may not be reliable in nonpapillary thyroid carcinomas, and the radiologist should keep in mind especially follicular or anaplastic carcinomas when evaluating score 2 or 3 lesions for recommendation of FNAB. Larger series are required to determine the stiffness of nonpapillary thyroid carcinoma. Although this study was not designed to evaluate the combination of B mode, Doppler mode, and elastography findings of nodules, we believe that adding B mode and Doppler mode findings may help in the final decision of these score 2 and 3 lesions. Thyroid elastography is shown to be applicable using freehand external compression or carotid artery pulsation as the compression source [17,20,35]. Carotid artery pulsation is reported to be a useful compression source, and the distance of the carotid artery from the lesion does not influence the diagnostic value [18,21]. Lyshchik et al. have reported an artifact occurring during freehand external compression caused by the interference of the off-plane motion and external compression by the carotid artery pulsation [17]. In our study, we used carotid artery pulsation rather than freehand compression to evaluate the elasticity, which precluded the described artifact [17]. Park et al. have investigated the interobserver correlation of US elastography [37]. Although significant correlation was found at various conventional US findings, significant correlation was not found in terms of US elastography. The main limitation of US elastography is that the magnitude of tissue compression affects both the strain image and the strain score [44]. In the current study, US elastography was performed by the first radiologist, who also scored the nodules during real-time evaluation. The second radiologist scored the nodules on the recorded video images. Our results showed moderate concordance (kappa: 0.51) between two radiologists’ assessment. From our results, it can be concluded that elastographic evaluation is observer dependent and scoring is best performed by the operator at real-time imaging. Our study had some limitations. First, FNAB results were accepted as gold standard in all benign lesions except in those with a final histopathological diagnosis; therefore, the limitations of FNAB also became the limitations of our study. Nondiagnostic or insufficient cytologic finding may constitute a problem, especially in cystic or vascular lesions; five of our patients were excluded from the study for this reason. Second, the number of malignant nodules (n=10) in our study was low compared to benign nodules (n= 93). Third, the nodules were classified as benign or malignant only. However, some

Please cite this article as: Akcay MA, et al, The value of ultrasound elastography in differentiation of malignancy in thyroid nodules, Clin Imaging (2013), http://dx.doi.org/10.1016/j.clinimag.2013.11.008

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types of benign nodules or the presence of underlying parenchymal pathology of the thyroid (such as Hashimoto’s thyroiditis) may also increase tissue stiffness [36]. The influence of nodule types or parenchymal disease was not evaluated in this study. In conclusion, US elastography is a promising imaging technique in differentiation of papillary thyroid carcinoma. Elastographic evaluation is observer dependent, and scoring is best performed by the operator at real-time imaging. Elastographic score 1 nodules may be accepted as benign, and we believe that FNAB is unnecessary in these lesions. Score 4 lesions have a high suspicion index of malignancy. Therefore, we recommend that FNAB should be performed in all nodules that display score 4 characteristics at elastography. Particularly in score 4 lesions, even if the FNAB result does not show malignancy, we believe that this should be considered as radiological– pathological discordance and repeat biopsies should be recommended. Although our series was not large enough, elastography alone did not seem to be reliable for recommendation of biopsy in score 2 and 3 lesions, and the decision of FNAB should be made clinically and radiologically in terms of each patient. Further prospective studies in larger series are required to determine whether there is a role for US elastography for discrimination of malignancy in score 2 and 3 lesions, especially in terms of nonpapillary thyroid carcinoma. References [1] Brauer RJ, Silver CE. Needle aspiration biopsy of thyroid nodules. Laryngoscope 1984;94:38–42. [2] Utiger RD. The multiplicity of thyroid nodules and carcinomas. N Engl J Med 2005;352:2376–8. [3] Brander A, Viikinkoski P, Nickels J, Kivisaari L. Thyroid gland: US screening in a random adult population. Radiology 1991;181:683–7. [4] Ezzat S, Sarti DA, Cain DR, Braunstein GD. Thyroid incidentalomas. Prevalence by palpation and ultrasonography. Arch Intern Med 1994;154:1838–40. [5] Koike E, Noguchi S, Yamashita H, Murakami T, Ohshima A, Kawamoto H, et al. Ultrasonographic characteristics of thyroid nodules: prediction of malignancy. Arch Surg 2001;136:334–7. [6] Gharib H, Goellner JR. Fine-needle aspiration biopsy of the thyroid: an appraisal. Ann Intern Med 1993;118:282–9. [7] Hegedüs L. Clinical practice. The thyroid nodule. N Engl J Med 2004;351:1764–71. [8] Takashima S, Fukuda H, Nomura N, Kishimoto H, Kim T, Kobayashi T. Thyroid nodules: re-evaluation with ultrasound. J Clin Ultrasound 1995;23:179–84. [9] Frates MC, Benson CB, Charboneau JW, Cibas ES, Clark OH, Coleman BG, et al. Society of Radiologists in Ultrasound. Management of thyroid nodules detected at US: Society of Radiologists in Ultrasound consensus conference statement. Radiology 2005;237:794–800. [10] Gharib H. Fine-needle aspiration biopsy of thyroid nodules: advantages, limitations, and effect. Mayo Clin Proc 1994;69:44–9. [11] Goellner JR, Gharib H, Grant CS, Johnson DA. Fine needle aspiration cytology of the thyroid, 1980 to 1986. Acta Cytol 1987;31:587–90. [12] Castro MR, Gharib H. Thyroid fine-needle aspiration biopsy: progress, practice, and pitfalls. Endocr Pract 2003;9:128–36. [13] Tan GH, Gharib H, Reading CC. Solitary thyroid nodule. Comparison between palpation and ultrasonography. Arch Intern Med 1995;155:2418–23. [14] Ophir J, Céspedes I, Ponnekanti H, Yazdi Y, Li X. Elastography: a quantitative method for imaging the elasticity of biological tissues. Ultrason Imaging 1991;13:111–34. [15] Garra BS, Cespedes EI, Ophir J, Spratt SR, Zuurbier RA, Magnant CM, et al. Elastography of breast lesions: initial clinical results. Radiology 1997;202:79–86. [16] Cochlin DL, Ganatra RH, Griffiths DF. Elastography in the detection of prostatic cancer. Clin Radiol 2002;57:1014–20. [17] Lyshchik A, Higashi T, Asato R, et al. Thyroid gland tumor diagnosis at US elastography. Radiology 2005;237:202–11.

[18] Rago T, Santini F, Scutari M, Pinchera A, Vitti P. Elastography: new developments in ultrasound for predicting malignancy in thyroid nodules. J Clin Endocrinol Metab 2007;92:2917–22. [19] Bae U, Dighe M, Dubinsky T, Minoshima S, Shamdasani V, Kim Y. Ultrasound thyroid elastography using carotid artery pulsation: preliminary study. J Ultrasound Med 2007 Jun;26:797–805. [20] Dighe M, Bae U, Richardson ML, Dubinsky TJ, Minoshima S, Kim Y. Differential diagnosis of thyroid nodules with US elastography using carotid artery pulsation. Radiology 2008;248:662–9. [21] Asteria C, Giovanardi A, Pizzocaro A, Cozzaglio L, Morabito A, Somalvico F, et al. US-elastography in the differential diagnosis of benign and malignant thyroid nodules. Thyroid 2008;18:523–31. [22] Itoh A, Ueno E, Tohno E, Kamma H, Takahashi H, Shiina T, et al. Breast disease: clinical application of US elastography for diagnosis. Radiology 2006;239:341–50. [23] Hamberger B, Gharib H, Melton LJ, Goellner JR, Zinsmeister AR. Fine-needle aspiration biopsy of thyroid nodules. Impact on thyroid practice and cost of care. Am J Med 1982;73:381–4. [24] Screaton NJ, Berman LH, Grant JW. US-guided core-needle biopsy of the thyroid gland. Radiology 2003;226:827–32. [25] Rago T, Vitti P, Chiovato L, Mazzeo S, De Liperi A, Miccoli P, et al. Role of conventional ultrasonography and color flow-doppler sonography in predicting malignancy in 'cold' thyroid nodules. Eur J Endocrinol 1998;138:41–6. [26] Papini E, Guglielmi R, Bianchini A, Crescenzi A, Taccogna S, Nardi F, et al. Risk of malignancy in nonpalpable thyroid nodules: predictive value of ultrasound and color-Doppler features. J Clin Endocrinol Metab 2002;87:1941–6. [27] Poller DN, Ibrahim AK, Cummings MH, Mikel JJ, Boote D, Perry M. Fine-needle aspiration of the thyroid. Cancer 2000;90:239–44. [28] Chow LS, Gharib H, Goellner JR, van Heerden JA. Nondiagnostic thyroid fine needle aspiration cytology: management dilemmas. Thyroid 2001;11:1147–51. [29] Greenleaf JF, Fatemi M, Insana M. Selected methods for imaging elastic properties of biological tissues. Annu Rev Biomed Eng 2003;5:57–78. [30] Carcangiu ML, Zampi G, Rosai J. Papillary thyroid carcinoma: a study of its many morphologic expressions and clinical correlates. Pathol Annu 1985;20:1–44. [31] Reading CC, Charboneau JW, Hay ID, Sebo TJ. Sonography of thyroid nodules: a "classic pattern" diagnostic approach. Ultrasound Q 2005;21:157–65. [32] McNicol AM. Pathology of thyroid tumours. Surgery (Oxf) 2007;25:458–62. [33] Thomas A, Fischer T, Frey H, Ohlinger R, Grunwald S, Blohmer JU, et al. Real-time elastography—an advanced method of ultrasound: first results in 108 patients with breast lesions. Ultrasound Obstet Gynecol 2006;28:335–40. [34] Giovannini M, Hookey LC, Bories E, Pesenti C, Monges G, Delpero JR. Endoscopic ultrasound elastography: the first step towards virtual biopsy? Preliminary results in 49 patients. Endoscopy 2006;38:344–8. [35] Dighe M, Kim J, Luo S, Kim Y. Utility of the ultrasound elastographic systolic thyroid stiffness index in reducing fine-needle aspirations. J Ultrasound Med 2010;29:565–74. [36] Hong Y, Liu X, Li Z, Zhang X, Chen M, Luo Z. Real-time ultrasound elastography in the differential diagnosis of benign and malignant thyroid nodules. J Ultrasound Med 2009;28:861–7. [37] Park SH, Kim SJ, Kim EK, Kim MJ, Son EJ, Kwak JY. Interobserver agreement in assessing the sonographic and elastographic features of malignant thyroid nodules. AJR Am J Roentgenol 2009;193:416–23. [38] Rago T, Vitti P. Role of thyroid ultrasound in the diagnostic evaluation of thyroid nodules. Best Pract Res Clin Endocrinol Metab 2008;22:913–28. [39] Bojunga J, Herrmann E, Meyer G, Weber S, Zeuzem S, Friedrich-Rust M. Real-time elastography for the differentiation of benignand malignant thyroid nodules: a metaanalysis. Thyroid 2010;20:1145–50. [40] Wang Y, Dan HJ, Dan HY, Li T, Hu B. Differential diagnosis of small single solid thyroid nodules using real-time ultrasound elastography. J Int Med Res 2010;38: 466–72. [41] Rubaltelli L, Corradin S, Dorigo A, Stabilito M, Tregnaghi A, Borsato S, et al. Differential diagnosis of benign and malignant thyroid nodules at elastosonography. Ultraschall Med 2009;30:175–9. [42] Rago T, Scutari M, Santini F, Loiacono V, Piaggi P, Di Coscio G, et al. Realtime elastosonography: useful tool for refining the presurgical diagnosis in thyroid nodules with indeterminate or nondiagnostic cytology. J Clin Endocrinol Metab 2010;95:5274–80. [43] Friedrich-Rust M, Sperber A, Holzer K, Diener J, Grünwald F, Badenhoop K, et al. Real-time elastography and contrastenhanced ultrasound for the assessment of thyroid nodules. Exp Clin Endocrinol Diabetes 2010;118:602–9. [44] Suen KC. Fine-needle aspiration biopsy of the thyroid. CMAJ 2002;167:491–5.

Please cite this article as: Akcay MA, et al, The value of ultrasound elastography in differentiation of malignancy in thyroid nodules, Clin Imaging (2013), http://dx.doi.org/10.1016/j.clinimag.2013.11.008

The value of ultrasound elastography in differentiation of malignancy in thyroid nodules.

We aimed to determine the value of ultrasound elastography (US-E) using carotid artery pulsation in differentiation of malignant and benign thyroid no...
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