{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,9]],"date-time":"2026-10-09T18:38:46Z","timestamp":1791571126161,"version":"4.3.4"},"reference-count":39,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2021,1,7]],"date-time":"2021-01-07T00:00:00Z","timestamp":1609977600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Oncol."],"abstract":"<jats:sec><jats:title>Objective<\/jats:title><jats:p>To investigate the diagnostic performance of contrast-enhanced ultrasound (CEUS) in the differentiation of primary thyroid lymphoma (PTL) and nodular Hashimoto\u2019s thyroiditis (NHT) in patients with background of heterogeneous diffuse Hashimoto\u2019s thyroiditis (HT).<\/jats:p><\/jats:sec><jats:sec><jats:title>Methods<\/jats:title><jats:p>Sixty HT patients with 64 thyroid nodules (31 PTL and 33 NHT) who had undergone CEUS examination were included in this study. With histopathological results as the reference, we evaluated the imaging features of each nodule on both conventional ultrasonography (US) and CEUS. Quantitative CEUS parameters including peak intensity (PI), time to peak (TTP), and area under the time\u2013intensity curve (AUC) were gathered in the nodule and background parenchyma. The ratio indexes of theses parameters were calculated by the ratio of the lesion and the corresponding thyroid parenchyma. Logistic regression and receiver operating characteristic (ROC) curves analyses of valuable US indicators were further preformed to evaluate the diagnostic capability of CEUS in discrimination of PTL and NHT.<\/jats:p><\/jats:sec><jats:sec><jats:title>Results<\/jats:title><jats:p>Among all the observed US imaging features and CEUS parameters, 10 indicators showed significant differences between PTL and NHT (all P &amp;lt; 0.05). All the significant indicators were ranked according to the odds ratios (ORs). Eight of them were CEUS associated including imaging features of enhancement pattern, degree, homogeneity, and quantification parameters of PI, AUC, ratios of PI, AUC, and TTP, while indicators on conventional US, including vascularity and size ranked the last two with ORs less than 3. The five single CEUS parameters showed good diagnostic performance in diagnosis of PTL with areas under ROC curves of 0.72\u20130.83 and accuracies of 70.3\u201375.0%. The combination of CEUS imaging features and the ratios of PI, AUC, and TTP demonstrated excellent diagnostic efficiency and achieved area under ROC curve of 0.92, which was significantly higher than any of the five single parameters (all P &amp;lt; 0.05), with a sensitivity of 83.9%, specificity of 87.9%, and accuracy of 85.9%.<\/jats:p><\/jats:sec><jats:sec><jats:title>Conclusions<\/jats:title><jats:p>CEUS is an efficient diagnostic tool in the differential diagnosis of PTL and NHT for patients with diffuse HT. Conjoint analysis of CEUS imaging features and quantification parameters could improve the diagnostic values.<\/jats:p><\/jats:sec>","DOI":"10.3389\/fonc.2020.597975","type":"journal-article","created":{"date-parts":[[2021,1,7]],"date-time":"2021-01-07T06:49:13Z","timestamp":1610002153000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":25,"title":["Contrast-Enhanced Ultrasound in the Differential Diagnosis of Primary Thyroid Lymphoma and Nodular Hashimoto\u2019s Thyroiditis in a Background of Heterogeneous Parenchyma"],"prefix":"10.3389","volume":"10","author":[{"given":"Lulu","family":"Yang","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Haina","family":"Zhao","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yushuang","family":"He","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xianglan","family":"Zhu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Can","family":"Yue","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yan","family":"Luo","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Buyun","family":"Ma","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2021,1,7]]},"reference":[{"key":"B1","doi-asserted-by":"publisher","DOI":"10.1056\/NEJMra021194","article-title":"Thyroiditis","volume":"348","author":"Pearce","year":"2003","journal-title":"N Engl J Med"},{"key":"B2","doi-asserted-by":"publisher","DOI":"10.1056\/NEJM198503073121001","article-title":"Cancer risks in patients with chronic lymphocytic thyroiditis","volume":"312","author":"Holm","year":"1985","journal-title":"N Engl J Med"},{"key":"B3","doi-asserted-by":"publisher","first-page":"994","DOI":"10.1634\/theoncologist.2013-0036","article-title":"Thyroid lymphoma: recent advances in diagnosis and optimal management strategies","volume":"18","author":"Walsh","year":"2013","journal-title":"Oncologist"},{"key":"B4","doi-asserted-by":"publisher","DOI":"10.1111\/j.1365-2141.2011.08606.x","article-title":"Clinicopathological features of 171 cases of primary thyroid lymphoma: a long-term study involving 24553 patients with Hashimoto\u2019s disease","volume":"153","author":"Watanabe","year":"2011","journal-title":"Br J Haematol"},{"key":"B5","doi-asserted-by":"publisher","DOI":"10.1097\/00000478-200005000-00001","article-title":"Malignant lymphoma of the thyroid gland: a clinicopathologic study of 108 cases","volume":"24","author":"Derringer","year":"2000","journal-title":"Am J Surg Pathol"},{"key":"B6","doi-asserted-by":"publisher","DOI":"10.1002\/jso.20691","article-title":"Anaplastic thyroid cancer and primary thyroid lymphoma: a review of these rare thyroid malignancies","volume":"94","author":"Green","year":"2006","journal-title":"J Surg Oncol"},{"key":"B7","doi-asserted-by":"publisher","DOI":"10.1210\/jc.2013-1428","article-title":"Primary thyroid lymphoma: a clinical review","volume":"98","author":"Stein","year":"2013","journal-title":"J Clin Endocrinol Metab"},{"key":"B8","doi-asserted-by":"publisher","DOI":"10.1002\/jso.21543","article-title":"Characteristics and prognosis of primary thyroid non-Hodgkin\u2019s lymphoma in Chinese patients","volume":"101","author":"Sun","year":"2010","journal-title":"J Surg Oncol"},{"key":"B9","doi-asserted-by":"publisher","DOI":"10.1007\/s10434-001-0338-4","article-title":"Clinical presentation and treatment of non-Hodgkin\u2019s lymphoma of the thyroid gland","volume":"8","author":"Wirtzfeld","year":"2001","journal-title":"Ann Surg Oncol"},{"key":"B10","doi-asserted-by":"publisher","DOI":"10.1089\/thy.2006.16.983","article-title":"Usefulness of ultrasonography for diagnosis of malignant lymphoma of the thyroid","volume":"16","author":"Ota","year":"2006","journal-title":"Thyroid"},{"key":"B11","doi-asserted-by":"publisher","DOI":"10.1089\/thy.2005.15.742","article-title":"Serial changes in thyroid ultrasonogram in a patient with Hashimoto\u2019s thyroiditis who developed malignant lymphoma","volume":"15","author":"Matsuzuka","year":"2005","journal-title":"Thyroid"},{"key":"B12","doi-asserted-by":"publisher","first-page":"199","DOI":"10.1016\/s0929-8266(98)00038-x","article-title":"Primary thyroid lymphoma associated with metastatic thyroid tumor: Discrimination with US","volume":"7","author":"Horii","year":"1998","journal-title":"Eur J Ultrasound"},{"key":"B13","doi-asserted-by":"publisher","first-page":"e114080","DOI":"10.1371\/journal.pone.0114080","article-title":"Sonographic appearance of primary thyroid lymphoma-preliminary experience","volume":"9","author":"Xia","year":"2014","journal-title":"PLoS One"},{"key":"B14","doi-asserted-by":"publisher","DOI":"10.21037\/jtd.2017.09.48","article-title":"Comparison of sonographic characteristics of primary thyroid lymphoma and anaplastic thyroid carcinoma","volume":"9","author":"Gu","year":"2017","journal-title":"J Thorac Dis"},{"key":"B15","doi-asserted-by":"publisher","DOI":"10.1016\/j.clinimag.2012.04.024","article-title":"Ultrasound of primary thyroid non-Hodgkin\u2019s lymphoma","volume":"38","author":"Ma","year":"2014","journal-title":"Clin Imaging"},{"key":"B16","doi-asserted-by":"publisher","DOI":"10.1007\/s00330-012-2385-6","article-title":"Quantitative evaluation of contrast-enhanced ultrasound after intravenous administration of a microbubble contrast agent for differentiation of benign and malignant thyroid nodules: assessment of diagnostic accuracy","volume":"22","author":"Nemec","year":"2012","journal-title":"Eur Radiol"},{"key":"B17","doi-asserted-by":"publisher","DOI":"10.3233\/CH-151966","article-title":"Contrast-enhanced ultrasound with perfusion analysis for the identification of malignant and benign tumours of the thyroid gland","volume":"63","author":"Wendl","year":"2016","journal-title":"Clin Hemorheol Microcirc"},{"key":"B18","doi-asserted-by":"publisher","DOI":"10.1007\/s12020-015-0850-0","article-title":"Diagnostic value of contrast-enhanced ultrasound in solid thyroid nodules with and without enhancement","volume":"53","author":"Wu","year":"2016","journal-title":"Endocrine"},{"key":"B19","doi-asserted-by":"publisher","DOI":"10.1089\/thy.2009.0045","article-title":"Utility of contrast-enhanced ultrasound for evaluation of thyroid nodules","volume":"20","author":"Zhang","year":"2010","journal-title":"Thyroid"},{"key":"B20","doi-asserted-by":"publisher","DOI":"10.1007\/s00330-016-4508-y","article-title":"Usefulness of combined use of contrast-enhanced ultrasound and TI-RADS classification for the differentiation of benign from malignant lesions of thyroid nodules","volume":"27","author":"Zhang","year":"2017","journal-title":"Eur Radiol"},{"key":"B21","article-title":"Diagnosis of chronic lymphocytic thyroiditis (nodular presentation) by needle aspiration","volume":"25","author":"Friedman","year":"1981","journal-title":"Acta Cytol"},{"key":"B22","doi-asserted-by":"publisher","DOI":"10.1148\/radiology.185.1.1523294","article-title":"Thyroid nodules associated with Hashimoto thyroiditis: assessment with US","volume":"185","author":"Takashima","year":"1992","journal-title":"Radiology"},{"key":"B23","doi-asserted-by":"publisher","DOI":"10.2214\/AJR.09.2459","article-title":"Hashimoto thyroiditis: Part 1, sonographic analysis of the nodular form of Hashimoto thyroiditis","volume":"195","author":"Anderson","year":"2010","journal-title":"Am J Roentgenol"},{"key":"B24","doi-asserted-by":"publisher","first-page":"45","DOI":"10.14366\/usg.14031","article-title":"A comparison of lymphocytic thyroiditis with papillary thyroid carcinoma showing suspicious ultrasonographic findings in a background of heterogeneous parenchyma","volume":"34","author":"Nam","year":"2015","journal-title":"Ultrasonography"},{"key":"B25","doi-asserted-by":"publisher","DOI":"10.7863\/jum.2012.31.11.1767","article-title":"Likelihood Ratio\u2013Based Differentiation of Nodular Hashimoto Thyroiditis and Papillary Thyroid Carcinoma in Patients With Sonographically Evident Diffuse Hashimoto Thyroiditis: Preliminary Study","volume":"31","author":"Wang","year":"2012","journal-title":"J Ultrasound Med"},{"key":"B26","doi-asserted-by":"publisher","DOI":"10.1182\/blood-2016-01-643569","article-title":"The 2016 revision of the World Health Organization classification of lymphoid neoplasms","volume":"127","author":"Swerdlow","year":"2016","journal-title":"Blood"},{"key":"B27","doi-asserted-by":"crossref","DOI":"10.2307\/2531595","article-title":"Comparing the areas under two or more correlated receiver operating characteristic curves: a nonparametric approach","volume":"44","author":"DeLong","year":"1988","journal-title":"Biometrics"},{"key":"B28","doi-asserted-by":"publisher","DOI":"10.1016\/j.surg.2009.09.020","article-title":"Prognosis of primary thyroid lymphoma: demographic, clinical, and pathologic predictors of survival in 1,408 cases","volume":"146","author":"Graff-Baker","year":"2009","journal-title":"Surgery"},{"key":"B29","doi-asserted-by":"publisher","first-page":"25","DOI":"10.1046\/j.1365-2559.1996.268311.x","article-title":"Primary non-Hodgkin\u2019s lymphoma of the thyroid gland: a population based study","volume":"28","author":"Pedersen","year":"1996","journal-title":"Histopathology"},{"key":"B30","doi-asserted-by":"publisher","DOI":"10.1080\/08941939.2017.1383536","article-title":"A review of primary thyroid lymphoma: molecular factors, diagnosis and management","volume":"32","author":"Pavlidis","year":"2019","journal-title":"J Invest Surg"},{"key":"B31","doi-asserted-by":"publisher","DOI":"10.7863\/jum.2012.31.4.589","article-title":"Thyroid lymphoma: correlation of radiologic and pathologic features","volume":"31","author":"Nam","year":"2012","journal-title":"J Ultrasound Med"},{"key":"B32","doi-asserted-by":"publisher","DOI":"10.7863\/ultra.34.2.317","article-title":"Primary thyroid lymphoma has different sonographic and color Doppler features compared to nodular goiter","volume":"34","author":"Wang","year":"2015","journal-title":"J Ultrasound Med"},{"key":"B33","doi-asserted-by":"publisher","DOI":"10.2214\/ajr.176.3.1760751","article-title":"Sonographic appearance of focal thyroiditis","volume":"176","author":"Langer","year":"2001","journal-title":"Am J Roentgenol"},{"key":"B34","doi-asserted-by":"publisher","DOI":"10.1089\/thy.2012.0554","article-title":"Hashimoto\u2019s thyroiditis: celebrating the centennial through the lens of the Johns Hopkins hospital surgical pathology records","volume":"23","author":"Caturegli","year":"2013","journal-title":"Thyroid"},{"key":"B35","doi-asserted-by":"publisher","DOI":"10.1016\/j.ejrad.2012.04.033","article-title":"Focal thyroid inferno\u201d on color Doppler ultrasonography: A specific feature of focal Hashimoto\u2019s thyroiditis","volume":"81","author":"Fu","year":"2012","journal-title":"Eur J Radiol"},{"key":"B36","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1089\/thy.2015.0020","article-title":"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","volume":"26","author":"Haugen","year":"2015","journal-title":"Thyroid"},{"key":"B37","doi-asserted-by":"publisher","DOI":"10.1089\/thy.2013.0150","article-title":"Diagnostic performances of various gray-scale, color Doppler, and contrast-enhanced ultrasonography findings in predicting malignant thyroid nodules","volume":"24","author":"Ma","year":"2014","journal-title":"Thyroid"},{"key":"B38","doi-asserted-by":"publisher","DOI":"10.1002\/jum.14347","article-title":"Diagnostic Efficiency of Quantitative Contrast-Enhanced Ultrasound Indicators for Discriminating Benign From Malignant Solid Thyroid Nodules","volume":"37","author":"Zhou","year":"2018","journal-title":"J Ultrasound Med"},{"key":"B39","doi-asserted-by":"publisher","first-page":"288","DOI":"10.14366\/usg.18019","article-title":"Application of contrast-enhanced ultrasound for evaluation of thyroid nodules","volume":"37","author":"Zhan","year":"2018","journal-title":"Ultrasonography"}],"container-title":["Frontiers in Oncology"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fonc.2020.597975\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2021,1,7]],"date-time":"2021-01-07T06:49:15Z","timestamp":1610002155000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fonc.2020.597975\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,1,7]]},"references-count":39,"alternative-id":["10.3389\/fonc.2020.597975"],"URL":"https:\/\/doi.org\/10.3389\/fonc.2020.597975","relation":{},"ISSN":["2234-943X"],"issn-type":[{"value":"2234-943X","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,1,7]]},"article-number":"597975"}}