{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,9]],"date-time":"2026-09-09T00:50:26Z","timestamp":1788915026856,"version":"build-2803163510"},"reference-count":33,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2022,7,22]],"date-time":"2022-07-22T00:00:00Z","timestamp":1658448000000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2022,7,22]],"date-time":"2022-07-22T00:00:00Z","timestamp":1658448000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"funder":[{"name":"Key Project of Scientific and Technological Innovation in Hangzhou","award":["20131813A08"],"award-info":[{"award-number":["20131813A08"]}]},{"name":"Medical Science Research Program of Zhejiang Province","award":["2020RC091, 2021RC024"],"award-info":[{"award-number":["2020RC091, 2021RC024"]}]},{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["81871337"],"award-info":[{"award-number":["81871337"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["BMC Endocr Disord"],"published-print":{"date-parts":[[2022,12]]},"abstract":"<jats:title>Abstract<\/jats:title><jats:sec>\n                <jats:title>Background<\/jats:title>\n                <jats:p>To investigate the diagnostic value of ultrasound gray scale ratio (UGSR) in differentiating papillary thyroid microcarcinomas (PTMCs) from benign micronodules (BMNs) in patients with Hashimoto\u2019s thyroiditis (HT).<\/jats:p>\n              <\/jats:sec><jats:sec>\n                <jats:title>Methods<\/jats:title>\n                <jats:p>The ultrasound images of 285 PTMCs (from 247 patients) and 173 BMNs (from 140 patients) in the HT group, as well as 461 PTMCs (from 417 patients) and 234 BMNs (from 197 patients) in the non-HT group were retrospectively analyzed. The diagnosis of all cases was confirmed by histopathological examinations. The gray scale values of the nodules and surrounding thyroid tissues were measured and subsequently the UGSRs were calculated. Receiver operating characteristic curve analysis was used to determine the area under the curve (AUC), optimal UGSR threshold, sensitivity and specificity in differentiating PTMCs and BMNs in the two groups.<\/jats:p>\n              <\/jats:sec><jats:sec>\n                <jats:title>Results<\/jats:title>\n                <jats:p>The UGSR of PTMC and BMN was 0.52\u2009\u00b1\u20090.12 and 0.85\u2009\u00b1\u20090.24 in the HT group (<jats:italic>P<\/jats:italic>\u2009&lt;\u20090.001), and 0.57\u2009\u00b1\u20090.13 and 0.87\u2009\u00b1\u20090.20 in the non-HT group (<jats:italic>P<\/jats:italic>\u2009&lt;\u20090.001), respectively. The difference in PTMC-UGSR was significant between the two groups (<jats:italic>P<\/jats:italic>\u2009&lt;\u20090.001), whereas BMN-UGSR did not differ between the two groups (<jats:italic>P<\/jats:italic>\u2009=\u20090.416). The AUC, optimal UGSR threshold, sensitivity and specificity of UGSR for differentiating PTMC and BMN in the HT and non-HT group were 0.890 versus\u00a00.901, 0.68 versus 0.72, 91.23% versus 90.67%, and 77.46% versus 82.05%, respectively.<\/jats:p>\n              <\/jats:sec><jats:sec>\n                <jats:title>Conclusions<\/jats:title>\n                <jats:p>The USGR of the HT group was lower than that of the non-HT group.<\/jats:p>\n                <jats:p>Moreover, UGSR exhibited important diagnostic value in differentiating PTMC from BMN in both HT and non-HT groups.<\/jats:p>\n              <\/jats:sec>","DOI":"10.1186\/s12902-022-01028-0","type":"journal-article","created":{"date-parts":[[2022,7,22]],"date-time":"2022-07-22T04:02:23Z","timestamp":1658462543000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":3,"title":["Ultrasound gray scale ratio for differential diagnosis of papillary thyroid microcarcinoma from benign micronodule in patients with Hashimoto\u2019s thyroiditis"],"prefix":"10.1186","volume":"22","author":[{"given":"Zhijiang","family":"Han","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lesi","family":"Xie","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Peiying","family":"Wei","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zhikai","family":"Lei","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zhongxiang","family":"Ding","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ming","family":"Zhang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2022,7,22]]},"reference":[{"issue":"3","key":"1028_CR1","doi-asserted-by":"publisher","first-page":"892","DOI":"10.1148\/radiol.11110206","volume":"260","author":"JY Kwak","year":"2011","unstructured":"Kwak JY, Han KH, Yoon JH, 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\u20139.","journal-title":"Radiology"},{"issue":"11","key":"1028_CR2","doi-asserted-by":"publisher","first-page":"1257","DOI":"10.1089\/thy.2008.0021","volume":"19","author":"JY Park","year":"2009","unstructured":"Park JY, Lee HJ, Jang HW, et al. A proposal for a thyroid imaging reporting and data system for ultrasound features of thyroid carcinoma. Thyroid. 2009;19(11):1257\u201364.","journal-title":"Thyroid"},{"issue":"5","key":"1028_CR3","doi-asserted-by":"publisher","first-page":"225","DOI":"10.1159\/000478927","volume":"6","author":"G Russ","year":"2017","unstructured":"Russ G, Bonnema SJ, Erdogan MF, Durante C, Ngu R, Leenhardt L. European Thyroid Association Guidelines for Ultrasound Malignancy Risk Stratification of Thyroid Nodules in Adults: The EU-TIRADS. Eur Thyroid J. 2017;6(5):225\u201337.","journal-title":"Eur Thyroid J"},{"issue":"7","key":"1028_CR4","doi-asserted-by":"publisher","first-page":"682","DOI":"10.1016\/j.eprac.2021.01.009","volume":"27","author":"F Zhang","year":"2021","unstructured":"Zhang F, Russell YX, Guber HA. Transverse and Longitudinal Ultrasound Location of Thyroid Nodules and Risk of Thyroid Cancer. Endocr Pract. 2021;27(7):682\u201390.","journal-title":"Endocr Pract"},{"key":"1028_CR5","doi-asserted-by":"publisher","first-page":"109050","DOI":"10.1016\/j.ejrad.2020.109050","volume":"129","author":"H Liu","year":"2020","unstructured":"Liu H, Ma AL, Zhou YS, et al. Variability in the interpretation of grey-scale ultrasound features in assessing thyroid nodules: A systematic review and meta-analysis. Eur J Radiol. 2020;129:109050.","journal-title":"Eur J Radiol"},{"issue":"27","key":"1028_CR6","doi-asserted-by":"publisher","DOI":"10.1097\/MD.0000000000001129","volume":"94","author":"G Grani","year":"2015","unstructured":"Grani G, D\u2019Alessandri M, Carbotta G, et al. Grey-Scale Analysis Improves the Ultrasonographic Evaluation of Thyroid Nodules. Medicine. 2015;94(27):e1129.","journal-title":"Medicine"},{"issue":"18","key":"1028_CR7","doi-asserted-by":"publisher","first-page":"7644","DOI":"10.1002\/cam4.2653","volume":"8","author":"X Chen","year":"2019","unstructured":"Chen X, Gao M, Hu L, Zhu J, Zhang S, Wei X. The diagnostic value of the ultrasound gray scale ratio for different sizes of thyroid nodules. Cancer Med. 2019;8(18):7644\u20139.","journal-title":"Cancer Med"},{"issue":"5","key":"1028_CR8","doi-asserted-by":"publisher","first-page":"507","DOI":"10.21037\/qims.2018.06.04","volume":"8","author":"Z Han","year":"2018","unstructured":"Han Z, Lei Z, Li M, Luo D, Ding J. Differential diagnosis value of the ultrasound gray scale ratio for papillary thyroid microcarcinomas and micronodular goiters. Quant Imaging Med Surg. 2018;8(5):507\u201313.","journal-title":"Quant Imaging Med Surg"},{"issue":"7","key":"1028_CR9","doi-asserted-by":"publisher","first-page":"1567","DOI":"10.4103\/jcrt.JCRT_1031_17","volume":"14","author":"ZK Lei","year":"2018","unstructured":"Lei ZK, Li MK, Luo DC, Han ZJ. The clinical significance of ultrasound grayscale ratio in differentiating markedly hypoechoic and anechoic minimal thyroid nodules. J Cancer Res Ther. 2018;14(7):1567\u201371.","journal-title":"J Cancer Res Ther"},{"key":"1028_CR10","doi-asserted-by":"publisher","DOI":"10.3389\/fonc.2020.625238","volume":"10","author":"Z Han","year":"2020","unstructured":"Han Z, Feng N, Lu Y, et al. A Control Study on the Value of the Ultrasound Grayscale Ratio for the Differential Diagnosis of Thyroid Micropapillary Carcinoma and Micronodular Goiter in Two Medical Centers. Front Oncol. 2020;10:625238.","journal-title":"Front Oncol"},{"issue":"10","key":"1028_CR11","doi-asserted-by":"publisher","first-page":"102649","DOI":"10.1016\/j.autrev.2020.102649","volume":"19","author":"M Ralli","year":"2020","unstructured":"Ralli M, Angeletti D, Fiore M, et al. Hashimoto\u2019s thyroiditis: An update on pathogenic mechanisms, diagnostic protocols, therapeutic strategies, and potential malignant transformation. Autoimmun Rev. 2020;19(10):102649.","journal-title":"Autoimmun Rev"},{"issue":"5","key":"1028_CR12","doi-asserted-by":"publisher","first-page":"539","DOI":"10.1530\/EJE-19-0424","volume":"181","author":"H Guan","year":"2019","unstructured":"Guan H, de Morais NS, Stuart J, et al. Discordance of serological and sonographic markers for Hashimoto\u2019s thyroiditis with gold standard histopathology. Eur J Endocrinol. 2019;181(5):539\u201344.","journal-title":"Eur J Endocrinol"},{"issue":"1","key":"1028_CR13","doi-asserted-by":"publisher","first-page":"247","DOI":"10.3349\/ymj.2014.55.1.247","volume":"55","author":"I Kim","year":"2014","unstructured":"Kim I, Kim EK, Yoon JH, et al. Diagnostic role of conventional ultrasonography and shearwave elastography in asymptomatic patients with diffuse thyroid disease: initial experience with 57 patients. Yonsei Med J. 2014;55(1):247\u201353.","journal-title":"Yonsei Med J"},{"issue":"3","key":"1028_CR14","doi-asserted-by":"publisher","first-page":"762","DOI":"10.1148\/radiol.2473070944","volume":"247","author":"WJ Moon","year":"2008","unstructured":"Moon WJ, Jung SL, Lee JH, et al. Benign and malignant thyroid nodules: US differentiation\u2013multicenter retrospective study. Radiology. 2008;247(3):762\u201370.","journal-title":"Radiology"},{"issue":"3","key":"1028_CR15","doi-asserted-by":"publisher","first-page":"906","DOI":"10.1245\/s10434-012-2830-4","volume":"20","author":"GR Kim","year":"2013","unstructured":"Kim GR, Kim MH, Moon HJ, Chung WY, Kwak JY, Kim EK. Sonographic characteristics suggesting papillary thyroid carcinoma according to nodule size. Ann Surg Oncol. 2013;20(3):906\u201313.","journal-title":"Ann Surg Oncol"},{"issue":"6","key":"1028_CR16","doi-asserted-by":"publisher","DOI":"10.1016\/j.beem.2019.101367","volume":"33","author":"F Ragusa","year":"2019","unstructured":"Ragusa F, Fallahi P, Elia G, et al. Hashimotos\u2019 thyroiditis: Epidemiology, pathogenesis, clinic and therapy. Best Pract Res Clin Endocrinol Metab. 2019;33(6): 101367.","journal-title":"Best Pract Res Clin Endocrinol Metab"},{"issue":"4","key":"1028_CR17","doi-asserted-by":"publisher","first-page":"697","DOI":"10.7863\/ultra.34.4.697","volume":"34","author":"SM Durfee","year":"2015","unstructured":"Durfee SM, Benson CB, Arthaud DM, Alexander EK, Frates MC. Sonographic appearance of thyroid cancer in patients with Hashimoto thyroiditis. J Ultrasound Med. 2015;34(4):697\u2013704.","journal-title":"J Ultrasound Med"},{"key":"1028_CR18","doi-asserted-by":"publisher","first-page":"1006","DOI":"10.2741\/4437","volume":"21","author":"G Wu","year":"2016","unstructured":"Wu G, Zou D, Cai H, Liu Y. Ultrasonography in the diagnosis of Hashimoto\u2019s thyroiditis. Front Biosci (Landmark Ed). 2016;21:1006\u201312.","journal-title":"Front Biosci (Landmark Ed)"},{"issue":"11","key":"1028_CR19","doi-asserted-by":"publisher","first-page":"5971","DOI":"10.1007\/s00330-019-06174-z","volume":"29","author":"JY Lee","year":"2019","unstructured":"Lee JY, Hong HS, Kim CH. Prognostic value of acoustic structure quantification in patients with Hashimoto\u2019s thyroiditis. Eur Radiol. 2019;29(11):5971\u201380.","journal-title":"Eur Radiol"},{"key":"1028_CR20","doi-asserted-by":"publisher","first-page":"330","DOI":"10.1186\/s12885-015-1352-4","volume":"15","author":"N Slijepcevic","year":"2015","unstructured":"Slijepcevic N, Zivaljevic V, Marinkovic J, Sipetic S, Diklic A, Paunovic I. Retrospective evaluation of the incidental finding of 403 papillary thyroid microcarcinomas in 2466 patients undergoing thyroid surgery for presumed benign thyroid disease. BMC Cancer. 2015;15:330.","journal-title":"BMC Cancer"},{"issue":"8","key":"1028_CR21","doi-asserted-by":"publisher","first-page":"873","DOI":"10.1089\/thy.2009.0118","volume":"20","author":"K Gul","year":"2010","unstructured":"Gul K, Dirikoc A, Kiyak G, et al. The association between thyroid carcinoma and Hashimoto\u2019s thyroiditis: the ultrasonographic and histopathologic characteristics of malignant nodules. Thyroid. 2010;20(8):873\u20138.","journal-title":"Thyroid"},{"issue":"1","key":"1028_CR22","doi-asserted-by":"publisher","first-page":"216","DOI":"10.2214\/AJR.09.3680","volume":"195","author":"L Anderson","year":"2010","unstructured":"Anderson L, Middleton WD, Teefey SA, et al. Hashimoto thyroiditis: Part 2, sonographic analysis of benign and malignant nodules in patients with diffuse Hashimoto thyroiditis. AJR Am J Roentgenol. 2010;195(1):216\u201322.","journal-title":"AJR Am J Roentgenol"},{"key":"1028_CR23","doi-asserted-by":"publisher","first-page":"109059","DOI":"10.1016\/j.ejrad.2020.109059","volume":"131","author":"D Wang","year":"2020","unstructured":"Wang D, Du LY, Sun JW, et al. Evaluation of thyroid nodules with coexistent Hashimoto\u2019s thyroiditis according to various ultrasound-based risk stratification systems: A retrospective research. Eur J Radiol. 2020;131:109059.","journal-title":"Eur J Radiol"},{"issue":"4","key":"1028_CR24","doi-asserted-by":"publisher","first-page":"356","DOI":"10.1007\/s12022-015-9401-8","volume":"26","author":"H Baser","year":"2015","unstructured":"Baser H, Ozdemir D, Cuhaci N, et al. Hashimoto\u2019s Thyroiditis Does Not Affect Ultrasonographical, Cytological, and Histopathological Features in Patients with Papillary Thyroid Carcinoma. Endocr Pathol. 2015;26(4):356\u201364.","journal-title":"Endocr Pathol"},{"issue":"2","key":"1028_CR25","doi-asserted-by":"publisher","first-page":"474","DOI":"10.1210\/jc.2012-2978","volume":"98","author":"B Jankovic","year":"2013","unstructured":"Jankovic B, Le KT, Hershman JM. Clinical Review: Hashimoto\u2019s thyroiditis and papillary thyroid carcinoma: is there a correlation? J Clin Endocrinol Metab. 2013;98(2):474\u201382.","journal-title":"J Clin Endocrinol Metab"},{"issue":"3","key":"1028_CR26","doi-asserted-by":"publisher","first-page":"452","DOI":"10.1089\/thy.2020.0317","volume":"31","author":"SR Chung","year":"2021","unstructured":"Chung SR, Choi YJ, Lee SS, et al. Interobserver Reproducibility in Sonographic Measurement of Diameter and Volume of Papillary Thyroid Microcarcinoma. Thyroid. 2021;31(3):452\u20138.","journal-title":"Thyroid"},{"issue":"3","key":"1028_CR27","doi-asserted-by":"publisher","first-page":"408","DOI":"10.1089\/thy.2019.0147","volume":"30","author":"M Zhang","year":"2020","unstructured":"Zhang M, Tufano RP, Russell JO, et al. Ultrasound-Guided Radiofrequency Ablation Versus Surgery for Low-Risk Papillary Thyroid Microcarcinoma: Results of Over 5 Years\u2019 Follow-Up. Thyroid. 2020;30(3):408\u201317.","journal-title":"Thyroid"},{"issue":"12","key":"1028_CR28","doi-asserted-by":"publisher","first-page":"1752","DOI":"10.1089\/thy.2020.0049","volume":"30","author":"DK Teng","year":"2020","unstructured":"Teng DK, Li WH, Du JR, Wang H, Yang DY, Wu XL. Effects of Microwave Ablation on Papillary Thyroid Microcarcinoma: A Five-Year Follow-Up Report. Thyroid. 2020;30(12):1752\u20138.","journal-title":"Thyroid"},{"issue":"11","key":"1028_CR29","doi-asserted-by":"publisher","first-page":"1653","DOI":"10.1089\/thy.2019.0100","volume":"29","author":"DH Lee","year":"2019","unstructured":"Lee DH, Kim YK, Yu HW, Choi JY, Park SY, Moon JH. Computed Tomography for Detecting Cervical Lymph Node Metastasis in Patients Who Have Papillary Thyroid Microcarcinoma with Tumor Characteristics Appropriate for Active Surveillance. Thyroid. 2019;29(11):1653\u20139.","journal-title":"Thyroid"},{"issue":"6","key":"1028_CR30","doi-asserted-by":"publisher","first-page":"811","DOI":"10.1111\/cen.14529","volume":"95","author":"R Sutherland","year":"2021","unstructured":"Sutherland R, Tsang V, Clifton-Bligh RJ, Gild ML. Papillary thyroid microcarcinoma: Is active surveillance always enough? Clin Endocrinol (Oxf). 2021;95(6):811\u20137.","journal-title":"Clin Endocrinol (Oxf)"},{"issue":"12","key":"1028_CR31","doi-asserted-by":"publisher","first-page":"1807","DOI":"10.1007\/s40618-020-01326-1","volume":"43","author":"JW Feng","year":"2020","unstructured":"Feng JW, Ye J, Wu WX, Qu Z, Qin AC, Jiang Y. Management of cN0 papillary thyroid microcarcinoma patients according to risk-scoring model for central lymph node metastasis and predictors of recurrence. J Endocrinol Invest. 2020;43(12):1807\u201317.","journal-title":"J Endocrinol Invest"},{"issue":"3","key":"1028_CR32","doi-asserted-by":"publisher","first-page":"1327","DOI":"10.1007\/s00405-016-4302-0","volume":"274","author":"LS Liu","year":"2017","unstructured":"Liu LS, Liang J, Li JH, et al. The incidence and risk factors for central lymph node metastasis in cN0 papillary thyroid microcarcinoma: a meta-analysis. Eur Arch Otorhinolaryngol. 2017;274(3):1327\u201338.","journal-title":"Eur Arch Otorhinolaryngol"},{"key":"1028_CR33","doi-asserted-by":"publisher","first-page":"597975","DOI":"10.3389\/fonc.2020.597975","volume":"10","author":"L Yang","year":"2020","unstructured":"Yang L, Zhao H, He Y, et al. Contrast-Enhanced Ultrasound in the Differential Diagnosis of Primary Thyroid Lymphoma and Nodular Hashimoto\u2019s Thyroiditis in a Background of Heterogeneous Parenchyma. Front Oncol. 2020;10:597975.","journal-title":"Front Oncol"}],"container-title":["BMC Endocrine Disorders"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1186\/s12902-022-01028-0.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/article\/10.1186\/s12902-022-01028-0\/fulltext.html","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1186\/s12902-022-01028-0.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,7,22]],"date-time":"2022-07-22T16:03:39Z","timestamp":1658505819000},"score":1,"resource":{"primary":{"URL":"https:\/\/bmcendocrdisord.biomedcentral.com\/articles\/10.1186\/s12902-022-01028-0"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,7,22]]},"references-count":33,"journal-issue":{"issue":"1","published-print":{"date-parts":[[2022,12]]}},"alternative-id":["1028"],"URL":"https:\/\/doi.org\/10.1186\/s12902-022-01028-0","relation":{},"ISSN":["1472-6823"],"issn-type":[{"value":"1472-6823","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,7,22]]},"assertion":[{"value":"20 January 2022","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"15 April 2022","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"22 July 2022","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Declarations"}},{"value":"This study was performed in accordance with the ethics guidelines of the Helsinki Declaration and approved by the ethics committee of Affiliated Hangzhou First People\u2019s Hospital, Zhejiang University School of Medicine. Due to the retrospective nature of the study and the use of anonymized patient data, written informed consent for participation was waived.","order":2,"name":"Ethics","group":{"name":"EthicsHeading","label":"Ethics approval and consent to participate"}},{"value":"Not applicable.","order":3,"name":"Ethics","group":{"name":"EthicsHeading","label":"Consent for publication"}},{"value":"The authors declare that there is no conflict of interest.","order":4,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}],"article-number":"187"}}