TSH receptor autoantibody immunoassay in patients with Graves' disease: Improvement of diagnostic accuracy over different generations of methods. Systematic review and meta-analysis
Abstract
Background TSH receptor antibodies (TRAb) are the diagnostic hallmark of Graves' disease (GD) and immunoassays for their detection have been available for more than 30 years over three generations of laboratory methods. Despite a growing body of data produced by clinical and laboratory research which demonstrates its elevated sensitivity and specificity, TRAb testing is poorly used for diagnosing GD. The aim of our systematic review and meta-analysis is to verify the diagnostic performance of TRAb detected with 2nd and 3rd generation immunoassay methods.Methods We searched for English articles using MEDLINE with the search terms "TSH receptor antibody assay", "TSH Receptor antibody tests" and "Graves' disease". We analyzed studies reporting on TSH receptor antibody tests performed by quantitative immunoassays, on untreated patients with GD as the index disease (sensitivity) and on a control group of either healthy subjects or patients affected by other thyroid diseases (specificity). A total of 681 titles were initially identified with the search strategy described. 560 publications were excluded based on abstract and title. Full-text review was undertaken as the next step on 111 publications providing data on TRAb testing; 58 articles were subsequently excluded because they did not include untreated GD patients, or used either bioassays or 1st generation immunoassays. 32 were also excluded because they included data only on sensitivity or only on specificity of the assay, or were duplicates. Finally, 21 articles were selected for meta-analysis. Extraction of data from selected articles was performed by two authors independently, using predefined criteria: the number of patients with GD and the number of healthy or diseased controls; specification of the analytical method used to detect TRAb; sensitivity and specificity of the assay.Results The meta-analysis showed that the overall pooled sensitivity and specificity of the 2nd and 3rd generation TRAb assays are 97.1% and 97.4%, and 98.3% and 99.2%, respectively, with little difference between the types of immunoassay methods employed (human or porcine receptor, manual or automated procedure). The likelihood of a TRAb-positive individual to have GD is 1367- to 3420-fold greater (depending upon the type of assay) compared to a TRAb-negative person.Conclusions Data from the meta-analysis showed that TRAb measured with 2nd and 3rd generation immunoassay methods have very high sensitivity and specificity in the diagnosis of GD. The difference between 2nd and 3rd generation methods is small and is equally useful. In contrast with recommendations made by clinical endocrinologists who are not familiar with the state of the art in diagnostic technologies of autoimmunology laboratories, we propose a wide application of these tests in clinical practice to screen all hyperthyroid patients.
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In the setting of overt thyrotoxicosis, newer TRAb binding and bioassays have a sensitivity of 96-97% and a specificity of 99% for Graves' disease.
“In the setting of overt thyrotoxicosis, newer TRAb binding and bioassays have a sensitivity of 96-97% and a specificity of 99% for GD (56,57).”
From 2016 American Thyroid Association Guidelines for Diagnosis and Management of Hyperthyroidism and Other Causes of Thyrotoxicosis (2016) · cites this paper as [57]
Cites
Preferred Reporting Items for Systematic Reviews and Meta-Analyses: the PRISMA statement
Moher, D., Liberati, A., Tetzlaff, J., Altman, D. G., & for the PRISMA Group (2009) · BMJ · doi:10.1136/bmj.b2535 · Cited by 83,823 · see citing works
Preferred reporting items for systematic reviews and meta-analyses: the PRISMA Statement.
(2009) · PubMed Central · Cited by 44,859 · see citing works
Preferred reporting items for systematic reviews and meta-analyses: The PRISMA statement
Moher, D., Liberati, A., Tetzlaff, J., Altman, D. G., & the PRISMA Group* (2009) · Annals of Internal Medicine · doi:10.7326/0003-4819-151-4-200908180-00135 · Cited by 37,554 · see citing works
DeGroot, L. J., Abalovich, M., Alexander, E. K., Amino, N., Barbour, L. A., Cobin, R. H., Eastman, C. J., Lazarus, J. H., Luton, D., Mandel, S. J., et al. (2012) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2011-2803 · Cited by 1,862 · see citing works
Laboratory Support for the Diagnosis and Monitoring of Thyroid Disease
(2003) · Thyroid · doi:10.1089/105072503321086962 · Cited by 1,212 · see citing works
Bahn, R. S., Burch, H. B., Cooper, D. S., Garber, J. R., Greenlee, M. C., Klein, I., Laurberg, P., McDougall, I. R., Montori, V. M., Rivkees, S. A., et al. (2011) · Endocrine Practice · doi:10.4158/ep.17.3.456 · Cited by 1,098 · see citing works
Abalovich, M., Amino, N., Barbour, L. A., Cobin, R. H., DeGroot, L. J., Glinoer, D., Mandel, S. J., & Stagnaro‐Green, A. (2007) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2007-0141 · Cited by 929 · see citing works
The American Thyroid Association and American Association of Clinical Endocrinologists Taskforce on Hyperthyroidism and Other Causes of Thyrotoxicosis, Bahn, R. S., Burch, H. B., Cooper, D. S., Garber, J. R., Greenlee, M. C., Klein, I., Laurberg, P., McDougall, I. R., Montori, V. M., et al. (2011) · Thyroid · doi:10.1089/thy.2010.0417 · Cited by 898 · see citing works
THYROID-STIMULATING IMMUNOGLOBULINS IN GRAVES' DISEASE
SMITH, B. (1974) · The Lancet · doi:10.1016/s0140-6736(74)91815-7 · Cited by 567 · see citing works
Costagliola, S., Morgenthaler, N. G., Hoermann, R., Badenhoop, K. W. J., Struck, J., Freitag, D., Poertl, S., Weglöhner, W., Hollidt, J. M., Quadbeck, B., et al. (1999) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.84.1.5415 · Cited by 341 · see citing works
Story, J. A., & Kritchevsky, D. (1981) · PubMed · Cited by 273 · see citing works
AN IMPROVED RADIORECEPTOR ASSAY FOR TSH RECEPTOR ANTIBODIES
Shewring, G., & Smith, B. R. (1982) · Clinical Endocrinology · doi:10.1111/j.1365-2265.1982.tb01607.x · Cited by 268 · see citing works
Human monoclonal thyroid stimulating autoantibody
Sanders, J. F., Evans, M., Premawardhana, L., Depraetere, H., Jeffreys, J., Richards, T., Furmaniak, J., & Smith, B. R. (2003) · The Lancet · doi:10.1016/s0140-6736(03)13866-4 · Cited by 173 · see citing works
Manley, S. W., Bourke, J. R., & HAWKER, R. W. (1974) · Journal of Endocrinology · doi:10.1677/joe.0.0610437 · Cited by 151 · see citing works
Smith, B. R., Sanders, J. F., & Furmaniak, J. (2007) · Thyroid · doi:10.1089/thy.2007.0239 · Cited by 143 · see citing works
A New Assay for Thyrotropin Receptor Autoantibodies
Smith, B. R., Bolton, J., Young, S., Collyer, A., Weeden, A., Bradbury, J., Weightman, D. R., Perros, P., Sanders, J. F., & Furmaniak, J. (2004) · Thyroid · doi:10.1089/thy.2004.14.830 · Cited by 128 · see citing works
Pedersen, I. B., Knudsen, N., Perrild, H., Ovesen, L., & Laurberg, P. (2001) · Clinical Endocrinology · doi:10.1046/j.1365-2265.2001.01347.x · Cited by 108 · see citing works
Detecting TSH-Receptor Antibodies with the Recombinant TBII Assay: Technical and Clinical Evaluation
Schott, M., Feldkamp, J., Bathan, C., Fritzen, R., Scherbaum, W., & Seißler, J. (2000) · Hormone and Metabolic Research · doi:10.1055/s-2007-978666 · Cited by 99 · see citing works
Bioassays for TSH-receptor autoantibodies: An update
Lytton, S. D., & Kahaly, G. J. (2010) · Autoimmunity Reviews · doi:10.1016/j.autrev.2010.08.018 · Cited by 96 · see citing works
CHARACTERIZATION OF THE LONG-ACTING THYROID STIMULATOR OF GRAVES' DISEASE
Meek, J. C., Jones, A. E., Lewis, U. J., & VanderLaan, W. P. (1964) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.52.2.342 · Cited by 91 · see citing works
Kamijo, K. (2003) · Endocrine Journal · doi:10.1507/endocrj.50.113 · Cited by 86 · see citing works
Clinical review about TRAb assay's history
Zöphel, K., Roggenbuck, D., & Schott, M. (2010) · Autoimmunity Reviews · doi:10.1016/j.autrev.2010.05.021 · Cited by 77 · see citing works
Schott, M., Hermsen, D. F., Broecker‐Preuss, M., Casati, M., Cámara, J., Eckstein, A. K., Gassner, D., Golla, R., Graeber, C., van Helden, J., et al. (2008) · Clinical Endocrinology · doi:10.1111/j.1365-2265.2008.03512.x · Cited by 74 · see citing works
The Interaction of TSH Receptor Autoantibodies with 125I-Labelled TSH Receptor
Sanders, J. F., Oda, Y., Roberts, S., Kiddie, A., Richards, T., Bolton, J., McGrath, V., Walters, S. E., Jaskólski, D., Furmaniak, J., et al. (1999) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.84.10.6071 · Cited by 69 · see citing works
Takasu, N., Oshiro, C., Akamine, H., Komiya, I., Nagata, A., Sato, Y., Yoshimura, H., & Ito, K. (1997) · Journal of Endocrinological Investigation · doi:10.1007/bf03348001 · Cited by 63 · see citing works
Hyperthyroid Graves' disease without detectable thyrotropin receptor antibodies.
Ilicki, A., Gamstedt, A., & Karlsson, F. A. (1992) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.74.5.1349025 · Cited by 62 · see citing works
Measurement of Thyroid-stimulating Hormone Receptor Autoantibodies by ELISA
Bolton, J., Sanders, J. F., Oda, Y., Chapman, C., Konno, R., Furmaniak, J., & Smith, B. R. (1999) · Clinical Chemistry · doi:10.1093/clinchem/45.12.2285 · Cited by 58 · see citing works
Kamijo, K., ISHIKAWA, K., & Tanaka, M. (2005) · Endocrine Journal · doi:10.1507/endocrj.52.525 · Cited by 53 · see citing works
The role of TSH receptor antibodies in the management of Graves' disease
Matthews, D. C., & Syed, A. A. (2011) · European Journal of Internal Medicine · doi:10.1016/j.ejim.2011.02.006 · Cited by 52 · see citing works
Kawai, K., Tamai, H., Matsubayashi, S., Mukuta, T., Morita, T., Kubo, C., & Kuma, K. (1995) · Clinical Endocrinology · doi:10.1111/j.1365-2265.1995.tb02919.x · Cited by 52 · see citing works
Techniques to quantify TSH receptor antibodies
Ajjan, R., & Weetman, A. (2008) · Nature Clinical Practice Endocrinology & Metabolism · doi:10.1038/ncpendmet0886 · Cited by 51 · see citing works
Noh, J. Y., Miyazaki, N., Ito, K., Takeda, K., Hiramatsu, S., Morita, S., Miyauchi, A., Murakami, T., Inomata, K., Noguchi, S., et al. (2008) · Thyroid · doi:10.1089/thy.2008.0119 · Cited by 44 · see citing works
Massart, C., Sapin, R., Gibassier, J., Agin, A., & d’Herbomez, M. (2008) · Clinical Chemistry · doi:10.1373/clinchem.2008.115162 · Cited by 40 · see citing works
Liu, C., Hermsen, D. F., Domberg, J., Graeber, C., Hautzel, H., Duan, Y., Xu, K., Liu, C. P., Mao, X., Cupisti, K., et al. (2008) · Hormone and Metabolic Research · doi:10.1055/s-2008-1077051 · Cited by 35 · see citing works
Pedersen, I. B., Handberg, A., Knudsen, N. J., Heickendorff, L., & Laurberg, P. (2010) · Thyroid · doi:10.1089/thy.2009.0105 · Cited by 34 · see citing works
Kamijo, K. (2010) · Endocrine Journal · doi:10.1507/endocrj.k10e-199 · Cited by 34 · see citing works
Autoantibodies to the Human Thyrotropin Receptor Are Not Species Specific
Davies, T. F. (1981) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-52-3-426 · Cited by 32 · see citing works
The clinical autoimmunologist and the laboratory autoimmunologist: The two sides of the coin
Tozzoli, R., & Bizzaro, N. (2012) · Autoimmunity Reviews · doi:10.1016/j.autrev.2012.02.011 · Cited by 31 · see citing works
Self-citationMukuta, T., Tamai, H., Oshima, A., Morita, T., Matsubayashi, S., Fukata, S., & Kuma, K. (1994) · Clinical Endocrinology · doi:10.1111/j.1365-2265.1994.tb02471.x · Cited by 31 · see citing works
Gupta, M. K. (2000) · Clinica Chimica Acta · doi:10.1016/s0009-8981(99)00235-1 · Cited by 29 · see citing works
Villalta, D., Orunesu, E., Tozzoli, R., Montagna, P., Pesce, G., Bizzaro, N., & Bagnasco, M. (2004) · Journal of Clinical Pathology · doi:10.1136/jcp.2003.012294 · Cited by 28 · see citing works
Self-citationTozzoli, R., Kodermaz, G., Villalta, D., Bagnasco, M., Pesce, G., & Bizzaro, N. (2010) · Autoimmunity Highlights · doi:10.1007/s13317-010-0014-4 · Cited by 27 · see citing works
Self-citationPearce, E. N., Hennessey, J. V., & McDermott, M. T. (2011) · Thyroid · doi:10.1089/thy.2011.0104 · Cited by 24 · see citing works
Detection of low titre TBII in patients with Graves’ disease using recombinant human TSH receptor
Morgenthaler, N. G., Nagata, A., Katayama, S., Bergmann, A., & Iitaka, M. (2002) · Clinical Endocrinology · doi:10.1046/j.1365-2265.2002.01577.x · Cited by 20 · see citing works
Syme, N. R., Toft, A. D., Stoddart, M., & Beckett, G. J. (2011) · Annals of Clinical Biochemistry International Journal of Laboratory Medicine · doi:10.1258/acb.2011.011013 · Cited by 20 · see citing works
Zöphel, K., Roggenbuck, D., von Landenberg, P., Wunderlich, G., Grüning, T., Kotzerke, J., Lackner, K. J., & Smith, B. R. (2009) · Hormone and Metabolic Research · doi:10.1055/s-0029-1241196 · Cited by 20 · see citing works
Continuously Increasing Sensitivity over Three Generations of TSH Receptor Autoantibody Assays
Zöphel, K., Roggenbuck, D., Wunderlich, G., & Schott, M. (2010) · Hormone and Metabolic Research · doi:10.1055/s-0030-1267171 · Cited by 19 · see citing works
Giovanella, L., Ceriani, L., & Garancini, S. (2001) · PubMed · Cited by 16 · see citing works
Dasgupta, S., & Savage, M. W. (2005) · International Journal of Clinical Practice · doi:10.1111/j.1742-1241.2005.00545.x · Cited by 12 · see citing works
On specificity of 2nd generation TSH receptor autoantibody measurements.
Zöphel, K., Grüning, T., Roggenbuck, D., Wunderlich, G., & Kotzerke, J. (2008) · PubMed · Cited by 10 · see citing works
Hamidi, S., Chen, C., McLachlan, S. M., & Rapoport, B. (2011) · Thyroid · doi:10.1089/thy.2011.0147 · Cited by 10 · see citing works
Aleksić, A., Aleksić, Ž., & Stojanović, M. (2009) · PubMed · Cited by 10 · see citing works
Clinical applications of assays for thyrotropin-receptor antibodies in Graves' disease.
Ginsberg, J., & Westarp, C. V. (1986) · PubMed · Cited by 8 · see citing works
Cardia, M., Lima, N., Knobel, M., & Medeiros-Neto, G. A. (2004) · Thyroid · doi:10.1089/105072504323030951 · Cited by 8 · see citing works
Anti-thyroid-stimulating hormone receptor antibodies determined by second-generation assay
Mankaï, A., Toumi, D., Chadli-Chaieb, M., Besbes, L. G., Saad, F., Ouertani, M., Sfar, H., Jeddi, M., Chaieb, L., & Ghédira, I. (2007) · Clinical Chemistry and Laboratory Medicine (CCLM) · doi:10.1515/cclm.2007.016 · Cited by 7 · see citing works
Iida, Y., Konishi, J., KASAGI, K., Kuma, K., & Torizuka, K. (1982) · Endocrinologia Japonica · doi:10.1507/endocrj1954.29.227 · Cited by 6 · see citing works
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Ross, D. S., Burch, H. B., Cooper, D. S., Greenlee, M. C., Laurberg, P., Maia, A. L., Rivkees, S. A., Samuels, M., Sosa, J. A., Stan, M. N., et al. (2016) · Thyroid® · doi:10.1089/thy.2016.0229 · Cited by 2,938 · see citing works
“In the setting of overt thyrotoxicosis, newer TRAb binding and bioassays have a sensitivity of 96–97% and a specificity of 99% for GD (56,57).”
BackgroundSmith, T. J., & Hegedűs, L. D. (2016) · New England Journal of Medicine · doi:10.1056/nejmra1510030 · Cited by 1,273 · see citing works
2018 European Thyroid Association Guideline for the Management of Graves’ Hyperthyroidism
Kahaly, G. J., Bartalena, L., Hegedüs, L., Leenhardt, L., Poppe, K. G., & Pearce, S. H. S. (2018) · European Thyroid Journal · doi:10.1159/000490384 · Cited by 982 · see citing works
De Leo, S., Lee, S. Y., & Braverman, L. E. (2016) · The Lancet · doi:10.1016/s0140-6736(16)00278-6 · Cited by 883 · see citing works
Chemokine (C–X–C motif) ligand (CXCL)10 in autoimmune diseases
Antonelli, A., Ferrari, S. M., Giuggioli, D., Ferrannini, E., Ferri, C., & Fallahi, P. (2014) · Autoimmunity Reviews · doi:10.1016/j.autrev.2013.10.010 · Cited by 595 · see citing works
Davies, T. F., Andersen, S., Latif, R., Nagayama, Y., Barbesino, G., Brito, M., Eckstein, A. K., Stagnaro‐Green, A., & Kahaly, G. J. (2020) · Nature Reviews Disease Primers · doi:10.1038/s41572-020-0184-y · Cited by 421 · see citing works
Diagnosis and management of Graves disease: a global overview
Bartalena, L. (2013) · Nature Reviews Endocrinology · doi:10.1038/nrendo.2013.193 · Cited by 299 · see citing works
Diagnosis and classification of Graves' disease
Menconi, F., Marcocci, C., & Marinò, M. (2014) · Autoimmunity Reviews · doi:10.1016/j.autrev.2014.01.013 · Cited by 277 · see citing works
Clinical Utility of TSH Receptor Antibodies
Barbesino, G., & Tomer, Y. (2013) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2012-4309 · Cited by 237 · see citing works
Management of Graves Thyroidal and Extrathyroidal Disease: An Update
Kahaly, G. J. (2020) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/clinem/dgaa646 · Cited by 231 · see citing works
A 2013 European survey of clinical practice patterns in the management of Graves' disease
Bartalena, L., Burch, H. B., Burman, K. D., & Kahaly, G. J. (2014) · Clinical Endocrinology · doi:10.1111/cen.12688 · Cited by 197 · see citing works
Mikoś, H., Mikoś, M., Obara-Moszyńska, M., & Niedziela, M. (2014) · Endokrynologia Polska · doi:10.5603/ep.2014.0021 · Cited by 140 · see citing works
Thyrotoxicosis: Diagnosis and Management
Sharma, A. R., & Stan, M. N. (2019) · Mayo Clinic Proceedings · doi:10.1016/j.mayocp.2018.10.011 · Cited by 114 · see citing works
TSH Receptor Antibodies: Relevance & Utility
Kahaly, G. J., Diana, T., & Olivo, P. D. (2020) · Endocrine Practice · doi:10.4158/ep-2019-0363 · Cited by 94 · see citing works
Testing, Monitoring, and Treatment of Thyroid Dysfunction in Pregnancy
Lee, S. Y., & Pearce, E. N. (2020) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/clinem/dgaa945 · Cited by 94 · see citing works
Diagnosis and management of thyrotoxicosis
Vaidya, B., & Pearce, S. H. S. (2014) · BMJ · doi:10.1136/bmj.g5128 · Cited by 90 · see citing works
Graves’ hyperthyroidism in pregnancy: a clinical review
Nguyen, C. T., Sasso, E. B., Barton, L., & Mestman, J. H. (2018) · Clinical Diabetes and Endocrinology · doi:10.1186/s40842-018-0054-7 · Cited by 94 · see citing works
Thyroid-Stimulating Hormone Receptor Antibodies in Pregnancy: Clinical Relevance
Bucci, I., Giuliani, C., & Napolitano, G. (2017) · Frontiers in Endocrinology · doi:10.3389/fendo.2017.00137 · Cited by 81 · see citing works
Scappaticcio, L., Trimboli, P., Keller, F., Imperiali, M., Piccardo, A., & Giovanella, L. (2019) · Clinical Endocrinology · doi:10.1111/cen.14130 · Cited by 76 · see citing works
Pathophysiology of thyroid-associated orbitopathy
Lee, A. C. H., & Kahaly, G. J. (2022) · Best Practice & Research Clinical Endocrinology & Metabolism · doi:10.1016/j.beem.2022.101620 · Cited by 75 · see citing works
Thyrotropin Receptor Antibodies—An Overview
Kotwal, A., & Stan, M. N. (2018) · Ophthalmic Plastic and Reconstructive Surgery · doi:10.1097/iop.0000000000001052 · Cited by 73 · see citing works
Graves’ Disease Induced by Immune Checkpoint Inhibitors: A Case Report and Review of the Literature
Brancatella, A., Viola, N., Brogioni, S., Montanelli, L., Sardella, C., Vitti, P., Marcocci, C., Lupi, I., & Latrofa, F. (2019) · European Thyroid Journal · doi:10.1159/000501824 · Cited by 69 · see citing works
Tozzoli, R., D’Aurizio, F., Villalta, D., & Giovanella, L. (2016) · Clinical Chemistry and Laboratory Medicine (CCLM) · doi:10.1515/cclm-2016-0197 · Cited by 68 · see citing works
Self-citationZhou, L., Liu, Y., Wang, F., Jia, Z., Zhou, J., Jiang, T., Petti, L., Chen, Y., Xiong, Q., & Wang, X. (2018) · Talanta · doi:10.1016/j.talanta.2018.05.070 · Cited by 63 · see citing works
Diana, T., & Kahaly, G. J. (2018) · Ophthalmic Plastic and Reconstructive Surgery · doi:10.1097/iop.0000000000001053 · Cited by 62 · see citing works
Iodoprophylaxis and thyroid autoimmunity: an update
Teti, C., Panciroli, M., Nazzari, E., Pesce, G., Mariotti, S., Olivieri, A., & Bagnasco, M. (2021) · Immunologic Research · doi:10.1007/s12026-021-09192-6 · Cited by 61 · see citing works
Self-citationInsights from a Prospective Follow-up of Thyroid Function and Autoimmunity among COVID-19 Survivors
Lui, D. T. W., Lee, C., Chow, W. S., Lee, A. C. H., Tam, A. R., Fong, C. H. Y., Law, C. Y., Leung, E. K. H., To, K. K., Tan, K. C. B., et al. (2021) · Endocrinology and Metabolism · doi:10.3803/enm.2021.983 · Cited by 61 · see citing works
Measuring TSH receptor antibody to influence treatment choices in Graves’ disease
Asha, H. S., & Abraham, P. (2017) · Clinical Endocrinology · doi:10.1111/cen.13327 · Cited by 61 · see citing works
Lata, K., Dutta, P., Sridhar, S., Rohilla, M., Srinivasan, A., Prashad, G. R. V., Shah, V. N., & Bhansali, A. (2013) · Endocrine Connections · doi:10.1530/ec-13-0012 · Cited by 60 · see citing works
Relapse following antithyroid drug therapy for Graves’ hyperthyroidism
Laurberg, P., Krejbjerg, A., & Andersen, S. L. (2014) · Current Opinion in Endocrinology, Diabetes & Obesity · doi:10.1097/med.0000000000000088 · Cited by 60 · see citing works
Holthoff, H., Goebel, S., Li, Z., Faßbender, J., Reimann, A., Zeibig, S., Lohse, M. J., Münch, G., & Ungerer, M. (2015) · Endocrinology · doi:10.1210/en.2014-1813 · Cited by 56 · see citing works
Wang, Z., Yang, H., Wang, M., Petti, L., Jiang, T., Jia, Z., Xie, S., & Zhou, J. (2018) · Colloids and Surfaces A Physicochemical and Engineering Aspects · doi:10.1016/j.colsurfa.2018.02.069 · Cited by 57 · see citing works
Ide, A., Amino, N., Kang, S., Yoshioka, W., Kudo, T., Nishihara, E., Ito, M., Nakamura, H., & Miyauchi, A. (2014) · Thyroid® · doi:10.1089/thy.2013.0585 · Cited by 56 · see citing works
Outcome Prediction of Treatment of Graves’ Hyperthyroidism with Antithyroid Drugs
Piantanida, E., Lai, A., Sassi, L., Gallo, D., Spreafico, E., Tanda, M. L., & Bartalena, L. (2015) · Hormone and Metabolic Research · doi:10.1055/s-0035-1555759 · Cited by 53 · see citing works
Ma, Y., Liu, H., Chen, Y., Du, Y., Gu, C., Zhao, Z., Si, H., Wei, G., Jiang, T., & Zhou, J. (2020) · ACS Applied Nano Materials · doi:10.1021/acsanm.0c00652 · Cited by 48 · see citing works
Kwon, H., Kim, W. G., Jang, E. K., Kim, M., Park, S., Jeon, M. J., Kim, T. Y., Ryu, J., Shong, Y. K., & Kim, W. B. (2016) · Endocrinology and Metabolism · doi:10.3803/enm.2016.31.2.300 · Cited by 40 · see citing works
Peak Systolic Velocity of Superior Thyroid Artery for the Differential Diagnosis of Thyrotoxicosis
Zhao, X., Chen, L., Li, L., Wang, Y., Wang, Y., Zhou, L., Zeng, F., Li, Y., Hu, R., & Liu, H. (2012) · PLoS ONE · doi:10.1371/journal.pone.0050051 · Cited by 39 · see citing works
Clinical diagnosis of Graves’ or non-Graves’ hyperthyroidism compared to TSH receptor antibody test
Bell, L., Hunter, L., Kyriacou, A., Mukherjee, A., & Syed, A. A. (2018) · Endocrine Connections · doi:10.1530/ec-18-0082 · Cited by 39 · see citing works
Thyrotropin Receptor Epitope and Human Leukocyte Antigen in Graves’ Disease
Inaba, H., DeGroot, L. J., & Akamizu, T. (2016) · Frontiers in Endocrinology · doi:10.3389/fendo.2016.00120 · Cited by 38 · see citing works
Autilio, C., Morelli, R., Locantore, P., Pontecorvi, A., Zuppi, C., & Carrozza, C. (2017) · Annals of Clinical Biochemistry International Journal of Laboratory Medicine · doi:10.1177/0004563217700655 · Cited by 37 · see citing works
Review of Mouse Models of Graves’ Disease and Orbitopathy—Novel Treatment by Induction of Tolerance
Ungerer, M., Faßbender, J., Li, Z., Münch, G., & Holthoff, H. (2016) · Clinical Reviews in Allergy & Immunology · doi:10.1007/s12016-016-8562-7 · Cited by 33 · see citing works
Ji, D. Y., Park, S. H., Park, S. J., Kim, K. H., Ku, C. R., Shin, D. Y., Yoon, J. S., Lee, D. Y., & Lee, E. J. (2018) · Scientific Reports · doi:10.1038/s41598-018-27600-0 · Cited by 33 · see citing works
Diagnostic procedure in suspected Graves’ disease
Goichot, B., Leenhardt, L., Massart, C., Raverot, V., Tramalloni, J., & Iraqi, H. (2018) · Annales d Endocrinologie · doi:10.1016/j.ando.2018.08.002 · Cited by 32 · see citing works
Kim, Y. A., Cho, S. W., Choi, H. S., Moon, S., Moon, J. H., Kim, K. W., Park, D. J., Yi, K. H., Park, Y. J., & Cho, B. Y. (2016) · Thyroid · doi:10.1089/thy.2016.0056 · Cited by 32 · see citing works
Davies, T. F., Laurberg, P., & Bahn, R. S. (2016) · Elsevier eBooks · doi:10.1016/b978-0-323-29738-7.00012-5 · Cited by 32 · see citing works
Holthoff, H., Li, Z., Faßbender, J., Reimann, A., Adler, K., Münch, G., & Ungerer, M. (2017) · Endocrinology · doi:10.1210/en.2016-1845 · Cited by 31 · see citing works
Struja, T., Jutzi, R., Imahorn, N., Kaeslin, M., Boesiger, F., Kutz, A., Mundwiler, E., Huber, A., KRAENZLIN, M. E., Müeller, B., et al. (2019) · BMC Endocrine Disorders · doi:10.1186/s12902-019-0363-6 · Cited by 31 · see citing works
Villalta, D., D’Aurizio, F., Re, M. D., Ricci, D., Latrofa, F., & Tozzoli, R. (2018) · Autoimmunity Highlights · doi:10.1007/s13317-018-0102-4 · Cited by 27 · see citing works
Self-citationAlemtuzumab Induced Thyroid Disease in Multiple Sclerosis: A Review and Approach to Management
Mahzari, M., Arnaout, A., & Freedman, M. S. (2015) · Canadian Journal of Neurological Sciences / Journal Canadien des Sciences Neurologiques · doi:10.1017/cjn.2015.48 · Cited by 26 · see citing works
Kim, J., Choi, M. S., Park, J. T., Park, H., Jang, H. W., Choe, J., Kim, J., Kim, J. S., Cho, Y. S., Choi, J. Y., et al. (2021) · Thyroid · doi:10.1089/thy.2020.0756 · Cited by 26 · see citing works
Negro, R., Attanasio, R., Grimaldi, F., Guglielmi, R., & Papini, E. (2016) · European Thyroid Journal · doi:10.1159/000444482 · Cited by 25 · see citing works
Chazova, I. E., Михайловна, Ч. Н., Blinova, N. V., Belaya, Z. E., Danilov, N. M., Elfimova, E. M., Litvin, A. Y., Rozhinskaya, L. Y., Sviridenko, N. Y., Швецов, М. Ю., et al. (2023) · Eurasian heart journal · doi:10.38109/2225-1685-2023-1-6-65 · Cited by 28 · see citing works
Management of Thyrotoxicosis: Preconception, Pregnancy, and the Postpartum Period
Pearce, E. N. (2018) · Endocrine Practice · doi:10.4158/ep-2018-0356 · Cited by 26 · see citing works
Thyroid disease: Using diagnostic tools effectively
Croker, E. E., McGrath, S. A., & Rowe, C. W. (2021) · Australian Journal of General Practice · doi:10.31128/ajgp-10-20-5693 · Cited by 23 · see citing works
Deligiorgi, M. V., Sagredou, S., Vakkas, L., & Trafalis, D. T. (2021) · Cancers · doi:10.3390/cancers13215277 · Cited by 22 · see citing works
Graves’ hyperthyroidism in pregnancy
Nguyen, C. T., & Mestman, J. H. (2019) · Current Opinion in Endocrinology Diabetes and Obesity · doi:10.1097/med.0000000000000492 · Cited by 21 · see citing works
Prasek, K., Płazińska, M. T., & Królicki, L. (2015) · Nuclear Medicine Review · doi:10.5603/nmr.2015.0026 · Cited by 19 · see citing works
Giuliani, C., Saji, M., Bucci, I., & Napolitano, G. (2016) · Frontiers in Endocrinology · doi:10.3389/fendo.2016.00103 · Cited by 19 · see citing works
Kim, J. J., Jeong, S.-H., Kim, B., Kim, D., & Jeong, S. H. (2019) · Scandinavian Journal of Clinical and Laboratory Investigation · doi:10.1080/00365513.2019.1658216 · Cited by 18 · see citing works
Autoimmune Thyroid Disorders in Autoimmune Addison Disease
Stokland, A. M., Ueland, G. Å., Lima, K., Grønning, K., Finnes, T. E., Svendsen, M., Tomkowicz, A., Holte, S. E., Sollid, S. T., Dębowska, A., et al. (2022) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/clinem/dgac089 · Cited by 18 · see citing works
Sugamata, Y., Uchiyama, R., Honda, T., Tanaka, T., Matsunaga, T., & Yoshino, T. (2013) · International Journal of Molecular Sciences · doi:10.3390/ijms140714426 · Cited by 18 · see citing works
Receptor autoimmunity: diagnostic and therapeutic implications
Tozzoli, R. (2020) · Autoimmunity Highlights · doi:10.1186/s13317-019-0125-5 · Cited by 17 · see citing works
Self-citationOrtega, J. M. L., Martínez, P. S., Acevedo-León, D., & Capell, N. E. (2022) · PLoS ONE · doi:10.1371/journal.pone.0270890 · Cited by 16 · see citing works
Thyroid stimulating receptor autoantibodies
Gao, Y., Qiu, L., Yu, S., & Cheng, X. (2024) · Clinica Chimica Acta · doi:10.1016/j.cca.2024.119700 · Cited by 15 · see citing works
Antithyroid drug therapy in pregnancy: a review of guideline recommendations
Khan, I. N., Okosieme, O. E., & Lazarus, J. H. (2017) · Expert Review of Endocrinology & Metabolism · doi:10.1080/17446651.2017.1338944 · Cited by 16 · see citing works
Sarangi, P. K., Parida, S., Mangaraj, S., Mohanty, B. K., Mohanty, J., & Swain, B. M. (2021) · Indian journal of radiology and imaging - new series/Indian journal of radiology and imaging/Indian Journal of Radiology & Imaging · doi:10.1055/s-0041-1734360 · Cited by 15 · see citing works
Current controversies in the management of Graves’ hyperthyroidism
Francis, N., Francis, T., Lazarus, J. H., & Okosieme, O. E. (2020) · Expert Review of Endocrinology & Metabolism · doi:10.1080/17446651.2020.1754192 · Cited by 16 · see citing works
Rethinking screening for thyroid autoimmunity in vitiligo
Liu, M., Murphy, E. J., & Amerson, E. H. (2016) · Journal of the American Academy of Dermatology · doi:10.1016/j.jaad.2016.04.029 · Cited by 15 · see citing works
Baek, H.-S., Lee, J., Jeong, C., Lee, J., Ha, J., Jo, K., Kim, M., Cho, J., Kang, M. I., & Lim, D. (2022) · Journal of the Endocrine Society · doi:10.1210/jendso/bvac023 · Cited by 14 · see citing works
Liu, T., Zhang, X., Li, L., Zhou, L., Chen, J., Li, M., Gao, Y., Zhou, X., Han, X., & Ji, L. (2022) · BMC Endocrine Disorders · doi:10.1186/s12902-022-01114-3 · Cited by 14 · see citing works
The role of laboratory medicine in the diagnosis of the hyperthyroidism
D’Aurizio, F. (2021) · The Quarterly Journal of Nuclear Medicine and Molecular Imaging · doi:10.23736/s1824-4785.21.03344-6 · Cited by 13 · see citing works
Liu, K., Fu, Y., Li, T., Liu, S., Chen, D., Zhao, C., Shi, Y., Cai, Y., Yang, T., & zheng, X. (2021) · Clinical Biochemistry · doi:10.1016/j.clinbiochem.2021.07.014 · Cited by 12 · see citing works
Sensitivity of three thyrotropin receptor antibody assays in thyroid-associated orbitopathy
Matutinović, M. S., Diana, T., Nedeljković-Beleslin, B., Ćirić, J., Žarković, M., Perović-Blagojević, I., Kahaly, G., & Ignjatović, S. (2021) · Journal of Medical Biochemistry · doi:10.5937/jomb0-34718 · Cited by 12 · see citing works
Thyrotropin receptor antibody: A novel risk indicator for pregnancy loss
Li, Y., Xu, T., Mo, Q., Fu, W., & Yao, C. (2018) · Clinical Biochemistry · doi:10.1016/j.clinbiochem.2018.11.017 · Cited by 12 · see citing works
Evaluation of the role of thyroid scintigraphy in the differential diagnosis of thyrotoxicosis
Perdomo, C. M., García‐Goñi, M., Sancho, L., Paricio, J. J., Lozano, M. D., de la Higuera, M., Currás, M., Arbizu, J., & Galofré, J. C. (2020) · Clinical Endocrinology · doi:10.1111/cen.14308 · Cited by 11 · see citing works
Tong, M., Ding, J., Huang, B., Chen, J., Wei, X., Li, Z., Shu, J., Hu, Z., Jiang, X., & Sheng, H. (2021) · Clinica Chimica Acta · doi:10.1016/j.cca.2021.06.017 · Cited by 11 · see citing works
Brancatella, A., Torregrossa, L., Viola, N., Sgrò, D., Casula, M., Basolo, F., Materazzi, G., Marinò, M., Marcocci, C., Santini, F., et al. (2023) · Journal of Endocrinological Investigation · doi:10.1007/s40618-023-02044-0 · Cited by 11 · see citing works
Harmonization in autoimmune thyroid disease diagnostics
Tozzoli, R., & Bizzaro, N. (2018) · Clinical Chemistry and Laboratory Medicine (CCLM) · doi:10.1515/cclm-2018-0037 · Cited by 11 · see citing works
Self-citationCase 38-2015: A 21-Year-Old Man with Fatigue and Weight Loss
Pallais, J. C., McInnis, M., Saylor, P. J., & Wu, R. I. (2015) · New England Journal of Medicine · doi:10.1056/nejmcpc1506821 · Cited by 9 · see citing works
Thyroid Ultrasonography: Much Ado About Nothing? A Provocative Analysis
Ovčariček, P. P., & Giovanella, L. (2025) · Cancers · doi:10.3390/cancers17111764 · Cited by 10 · see citing works
Irisin and Myostatin Levels in Patients with Graves' Disease
Yalçın, M. M., Aktürk, M., Tohma, Y., Cerit, E. T., Altınova, A. E., Arslan, E., Yetkin, İ., & Törüner, F. B. (2016) · Archives of Medical Research · doi:10.1016/j.arcmed.2016.11.002 · Cited by 10 · see citing works
Higgins, V., Patel, K., Kulasingam, V., Beriault, D. R., Rutledge, A. C., & Selvaratnam, R. (2020) · Clinical Biochemistry · doi:10.1016/j.clinbiochem.2020.08.007 · Cited by 10 · see citing works
de Morais, N. S., Angell, T. E., Ahmadi, S., Alexander, E. K., Teixeira, P. D. F. D. S., & Marqusee, E. (2022) · Endocrine Practice · doi:10.1016/j.eprac.2022.01.007 · Cited by 10 · see citing works
Schwiebert, C., Kühnen, P., Becker, N., Welsink, T., Keller, T., Minich, W. B., Wiegand, S., & Schomburg, L. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21020463 · Cited by 10 · see citing works
Thyrotoxicosis after COVID-19 Infection with a Delay in Graves’ Disease Antibody Positivity
Boyle, D., & Mullally, J. A. (2023) · Case Reports in Endocrinology · doi:10.1155/2023/8402725 · Cited by 9 · see citing works
Spencer‐Bonilla, G., Ospina, N. S., Rodríguez‐Gutiérrez, R., Brito, J. P., Iñiguez‐Ariza, N. M., Tamhane, S. U., Erwin, P. J., Murad, M. H., & Montori, V. M. (2017) · Endocrine · doi:10.1007/s12020-017-1298-1 · Cited by 9 · see citing works
Hötte, G. J., de Bie, M., de Keizer, R. O. B., Kolijn, P. M., Drexhage, R. C., Veenbergen, S., Versnel, M. A., van Hagen, P. M., Paridaens, D. A., & Dik, W. A. (2024) · Frontiers in Endocrinology · doi:10.3389/fendo.2024.1469179 · Cited by 8 · see citing works
Stan, M. N., Algeciras‐Schimnich, A., Murthy, V., Thapa, P. B., & Araki, N. (2021) · Thyroid · doi:10.1089/thy.2021.0299 · Cited by 8 · see citing works
Quinn, M., Bashari, W. A., Smith, D., Gurnell, M., & Agha, A. (2020) · BMC Endocrine Disorders · doi:10.1186/s12902-020-00611-7 · Cited by 8 · see citing works
Hu, Y., Ni, J., Cen, Y., Zhang, B., Wu, W., Cheng, W., Huang, M., & Guan, M. (2021) · Journal of Clinical Laboratory Analysis · doi:10.1002/jcla.23950 · Cited by 8 · see citing works
Baek, H.-S., Kim, J., Jeong, C., Lee, J., Ha, J., Jo, K., Kim, M., Sohn, T. S., Lee, I. S., Lee, J. M., et al. (2024) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/clinem/dgae254 · Cited by 7 · see citing works
Bizzaro, N., Bagnasco, M., Tozzoli, R., Brusca, I., Cinquanta, L., Tampoia, M., Deleonardi, G., Antico, A., Pesce, G., Alessio, M. G., et al. (2018) · La Rivista Italiana della Medicina di Laboratorio - Italian Journal of Laboratory Medicine · doi:10.1007/s13631-018-0181-2 · Cited by 7 · see citing works
Self-citationFadeev, V. V. (2020) · Clinical and experimental thyroidology · doi:10.14341/ket12474 · Cited by 8 · see citing works
Wu, Z., Zhu, Y. M., Zhang, M., Wang, C., Zhou, L., Liu, W., Yang, W., Li, M., Zhang, S., Ren, Q., et al. (2021) · Frontiers in Endocrinology · doi:10.3389/fendo.2020.620407 · Cited by 7 · see citing works
Positive Thyrotropin Receptor Antibodies in Patients with Transient Thyrotoxicosis
Angell, T. E., Benschoten, O. V., Cohen, D. A., Haas, A. V., Alexander, E. K., & Marqusee, E. (2018) · Endocrine Practice · doi:10.4158/ep-2018-0059 · Cited by 7 · see citing works
Klit, F. Ø., Dal, J., Andersen, S. L., Nikontovic, A., Vestergaard, P., & Karmisholt, J. (2024) · Clinical Epidemiology · doi:10.2147/clep.s484335 · Cited by 6 · see citing works
Gan, D., Gao, T., Ma, L., Lü, H., Dai, H., Liu, Q.-Y., Lai, Y., Xin-hui, L., Peng, Z.-D., Chen, R.-Y., et al. (2024) · Journal of Ethnopharmacology · doi:10.1016/j.jep.2024.119106 · Cited by 6 · see citing works
Kalra, S., Selim, S., Shrestha, D., Somasundaram, N. P., Raza, S. A., Baruah, M., Bhattacharya, S., GADVE, S. S., Bantwal, G., & Sahay, R. K. (2024) · BMC Endocrine Disorders · doi:10.1186/s12902-024-01809-9 · Cited by 7 · see citing works
Applications of Cell-Based Bioassays Measuring The Induced Expression of Endogenous Genes
Moore, M. L., Ferguson, J., & Burns, C. J. (2014) · Bioanalysis · doi:10.4155/bio.14.98 · Cited by 6 · see citing works
Thyrotropin Receptor Antibodies
Tozzoli, R., Bagnasco, M., & Villalta, D. (2014) · Elsevier eBooks · doi:10.1016/b978-0-444-56378-1.00045-9 · Cited by 6 · see citing works
Self-citation
- Authors
- Tozzoli, R., Bagnasco, M., Giavarina, D., & Bizzaro, N.
- Affiliations
- Azienda Ospedaliera Santa Maria Degli Angeli (IT)
- University of Genoa (IT)
- Ospedale San Bortolo (IT)
- Venue
- Autoimmunity Reviews
- Publisher
- Elsevier BV
- Published
- 2012-12
- Volume
- 12
- Issue
- 2
- Pages
- 107-113
- ISSN
- 1568-9972 (ISSN-L)
- OpenAlex
- W1967526742
- Cited by
- 195
- References
- 56
- Citations by year
- 2026: 5 · 2025: 12 · 2024: 16 · 2023: 12 · 2022: 22 · 2021: 27 · 2020: 20 · 2019: 11 · 2018: 19 · 2017: 7 · 2016: 19 · 2015: 7 · 2014: 8 · 2013: 9 · 2012: 1
- FWCI
- 1.10
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Autoimmunity Reviews (publishedVersion)
- PubMed (publishedVersion)
- CINECA IRIS Institutial Research Information System (University of Genoa) (submittedVersion)
- Topics
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Thyroid Disorders and Treatments
- Health Sciences › Medicine › Pathology and Forensic Medicine › Ophthalmology and Eye Disorders
- Health Sciences › Medicine › Neurology › Myasthenia Gravis and Thymoma
- Keywords
- TSH receptor antibodies, Graves' disease, diagnostic accuracy, sensitivity and specificity, automated immunoassay, diagnostic performance, thyroid autoimmunity
- MeSH terms
- Autoantibodies, Graves Disease, Humans, Immunologic Tests, Receptors, Thyrotropin, Sensitivity and Specificity, Reproducibility of Results, Odds Ratio
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