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Multiparametric ultrasonography and ultrasound elastography in the differentiation of parathyroid lesions from ectopic thyroid lesions or lymphadenopathies

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Abstract

To evaluate the accuracy of ultrasound elastography with ElastoscanTM Core Index in the differential diagnosis of parathyroid lesions from ectopic thyroid nodules and lymph nodes. Seventy nine patients with repeatedly high levels of circulating intact parathyroid hormone, normal vitamin D and renal function tests, with an ultrasound scan showing a neck lesion, sharply demarcated from the thyroid lobules, were consecutively enrolled. Ultrasound with and without Color Doppler and ultrasound elastography were performed before histological examination. All ultrasound features, vascularization and ultrasound elastography diagnostic performance were assessed using ROC curves. Histological examination confirmed 47 parathyroid lesions, 18 thyroid ectopic nodules and 14 reactive lymph nodes. In distinguishing parathyroid from thyroid nodules, shape had a 100 % sensitivity (95 % CI 92.4–100) and 50 % specificity (95 % CI 37.2–64.7), cleavage had a 85.1 % sensitivity (95 % CI 72.3–92.6) and 77.8 % specificity (95 % CI 65.1–88) while peripheral vascularization had a sensitivity of 91.5 (95 % CI 79.6–97.6) and specificity of 72.2 (95 % CI 46.5–90.3). An ElastoscanTM Core Indexof 1.28 was 46 % sensitive (95 % CI 33.4–58.7) and 77 % specific (95 % CI 66.2–89.1) in discriminating parathyroid lesions from thyroid nodules. An ElastoscanTM Core Index of 1.0 was 78 % sensitive (95 % CI 65.1–88) and 71 % specific (95 % CI 56–81.3) in discriminating parathyroid lesions from lymph nodes (p = 0.045). An ElastoscanTM Core Index greater than 2.58 had a 100 % sensitivity (95 % CI 43.8–100) and 95.4 % specificity (95 % CI 38.3–99.7) in discriminating malignant from benign parathyroid nodules. ElastoscanTM Core Index was significantly higher in thyroid nodules than in reactive lymph nodes (1.18 ± 0.62, p = 0.008). The ultrasound features of cleavage and peripheral vascularization help to differentiate parathyroid from thyroid nodules. ElastoscanTM Core Index can improve ultrasound discrimination of parathyroid lesions from lymph nodes. The ElastoscanTM Core Index is significantly higher in malignant than in benign parathyroid lesions.

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Reference

  1. M. Barczynski, S. Cichon, A. Konturek, W. Cichon, Minimally invasive video-assisted parathyroidectomy versus open minimally invasive parathyroidectomy for a solitary parathyroid adenoma: a prospective, randomized, blinded trial. World. J. Surg. 30(5), 721–731 (2006). doi:10.1007/s00268-005-0312-6

    Article  PubMed  Google Scholar 

  2. C.S. Grant, G. Thompson, D. Farley, J. van Heerden, Primary hyperparathyroidism surgical management since the introduction of minimally invasive parathyroidectomy: Mayo Clinic experience. Arch. Surg. 140(5), 472–478 (2005). doi:10.1001/archsurg.140.5.472. discussion 478-479

    Article  PubMed  Google Scholar 

  3. G.M. Vitetta, P. Neri, A. Chiecchio, A. Carriero, S. Cirillo, A.B. Mussetto, A. Codegone, Role of ultrasonography in the management of patients with primary hyperparathyroidism: retrospective comparison with technetium-99m sestamibi scintigraphy. J. Ultrasound 17(1), 1–12 (2014). doi:10.1007/s40477-014-0067-8

    Article  PubMed  PubMed Central  Google Scholar 

  4. E. Hindie, O. Ugur, D. Fuster, M. O’Doherty, G. Grassetto, P. Urena, A. Kettle, S.A. Gulec, F. Pons, D. Rubello, Parathyroid Task Group of the, E.: 2009 EANM parathyroid guidelines. Eur. J. Nucl. Med. Mol. Imaging 36(7), 1201–1216 (2009). doi:10.1007/s00259-009-1131-z

    Article  PubMed  Google Scholar 

  5. C.N. Patel, H.M. Salahudeen, M. Lansdown, A.F. Scarsbrook, Clinical utility of ultrasound and 99mTc sestamibi SPECT/CT for preoperative localization of parathyroid adenoma in patients with primary hyperparathyroidism. Clin. Radiol. 65(4), 278–287 (2010). doi:10.1016/j.crad.2009.12.005

    Article  CAS  PubMed  Google Scholar 

  6. V. Cantisani, M. Bertolotto, H.P. Weskott, L. Romanini, H. Grazhdani, M. Passamonti, F.M. Drudi, F. Malpassini, A. Isidori, F.M. Meloni, F. Calliada, F. D’Ambrosio, Growing indications for CEUS: The kidney, testis, lymph nodes, thyroid, prostate, and small bowel. Eur. J. Radiol. 84(9), 1675–1684 (2015). doi:10.1016/j.ejrad.2015.05.008

    Article  CAS  PubMed  Google Scholar 

  7. V. Cantisani, H. Grazhdani, P. Ricci, K. Mortele, M. Di Segni, V. D’Andrea, A. Redler, G. Di Rocco, L. Giacomelli, E. Maggini, C. Chiesa, S.M. Erturk, S. Sorrenti, C. Catalano, F. D’Ambrosio, Q-elastosonography of solid thyroid nodules: assessment of diagnostic efficacy and interobserver variability in a large patient cohort. Eur. Radiol. 24(1), 143–150 (2014). doi:10.1007/s00330-013-2991-y

    Article  PubMed  Google Scholar 

  8. V. Cantisani, P. Lodise, G. Di Rocco, H. Grazhdani, D. Giannotti, G. Patrizi, E. Medvedyeva, M. Olive, C. Fioravanti, L. Giacomelli, C. Chiesa, A. Redler, C. Catalano, F. D’Ambrosio, P. Ricci, Diagnostic accuracy and interobserver agreement of Quasistatic Ultrasound Elastography in the diagnosis of thyroid nodules. Ultraschall Med. 36(2), 162–167 (2015). doi:10.1055/s-0034-1366467

    CAS  PubMed  Google Scholar 

  9. V. Cantisani, P. Lodise, H. Grazhdani, E. Mancuso, E. Maggini, G. Di Rocco, F. D’Ambrosio, F. Calliada, A. Redler, P. Ricci, C. Catalano, Ultrasound elastography in the evaluation of thyroid pathology. Current status. Eur. J. Radiol. 83(3), 420–428 (2014). doi:10.1016/j.ejrad.2013.05.008

    Article  PubMed  Google Scholar 

  10. M. Dighe, S. Luo, C. Cuevas, Y. Kim, Efficacy of thyroid ultrasound elastography in differential diagnosis of small thyroid nodules. Eur. J. Radiol. 82(6), e274–e280 (2013). doi:10.1016/j.ejrad.2013.01.009

    Article  PubMed  Google Scholar 

  11. C. Pozza, D. Gianfrilli, G. Fattorini, E. Giannetta, F. Barbagallo, E. Nicolai, C. Cristini, G.B. Di Pierro, G. Franco, A. Lenzi, P.S. Sidhu, V. Cantisani, A.M. Isidori, Diagnostic value of qualitative and strain ratio elastography in the differential diagnosis of non-palpable testicular lesions. Andrology (2016). doi:10.1111/andr.12260

  12. V. Cantisani, F. Consorti, A. Guerrisi, I. Guerrisi, P. Ricci, M. Di Segni, E. Mancuso, L. Scardella, F. Milazzo, F. D’Ambrosio, A. Antonaci, Prospective comparative evaluation of quantitative-elastosonography (Q-elastography) and contrast-enhanced ultrasound for the evaluation of thyroid nodules: preliminary experience. Eur. J. Radiol. 82(11), 1892–1898 (2013). doi:10.1016/j.ejrad.2013.07.005

    Article  CAS  PubMed  Google Scholar 

  13. D. Carlson, Parathyroid pathology: hyperparathyroidism and parathyroid tumors. Arch. Pathol. Lab. Med. 134(11), 1639–1644 (2010). doi:10.1043/2009-0578-CCR.1

    PubMed  Google Scholar 

  14. C. Asteria, A. Giovanardi, A. Pizzocaro, L. Cozzaglio, A. Morabito, F. Somalvico, A. Zoppo, US-elastography in the differential diagnosis of benign and malignant thyroid nodules. Thyroid 18(5), 523–531 (2008). doi:10.1089/thy.2007.0323

    Article  PubMed  Google Scholar 

  15. T. Rago, M. Scutari, F. Santini, V. Loiacono, P. Piaggi, G. Di Coscio, F. Basolo, P. Berti, A. Pinchera, P. Vitti, Real-time elastosonography: useful tool for refining the presurgical diagnosis in thyroid nodules with indeterminate or nondiagnostic cytology. J. Clin. Endocrinol. Metab. 95(12), 5274–5280 (2010). doi:10.1210/jc.2010-0901

    Article  CAS  PubMed  Google Scholar 

  16. U. Unluturk, M.F. Erdogan, O. Demir, C. Culha, S. Gullu, N. Baskal, The role of ultrasound elastography in preoperative localization of parathyroid lesions: a new assisting method to preoperative parathyroid ultrasonography. Clin. Endocrinol. (Oxf). 76(4), 492–498 (2012). doi:10.1111/j.1365-2265.2011.04241.x

    Article  PubMed  Google Scholar 

  17. S. Rickes, J. Sitzy, H. Neye, K.W. Ocran, W. Wermke, High-resolution ultrasound in combination with colour-Doppler sonography for preoperative localization of parathyroid adenomas in patients with primary hyperparathyroidism. Ultraschall Med. 24(2), 85–89 (2003). doi:10.1055/s-2003-38667

    Article  CAS  PubMed  Google Scholar 

  18. D. Cosgrove, F. Piscaglia, J. Bamber, J. Bojunga, J.M. Correas, O.H. Gilja, A.S. Klauser, I. Sporea, F. Calliada, V. Cantisani, M. D’Onofrio, E.E. Drakonaki, M. Fink, M. Friedrich-Rust, J. Fromageau, R.F. Havre, C. Jenssen, R. Ohlinger, A. Saftoiu, F. Schaefer, C.F. Dietrich, Efsumb: EFSUMB guidelines and recommendations on the clinical use of ultrasound elastography. Part 2: Clinical applications. Ultraschall Med. 34(3), 238–253 (2013). doi:10.1055/s-0033-1335375

    Article  CAS  PubMed  Google Scholar 

  19. M.W. Seybt, D.J. Terris, Minimally invasive thyroid and parathyroid surgery: where are we now and where are we going? Otolaryngol. Clin. North. Am. 43(2), 375–380 (2010). doi:10.1016/j.otc.2010.02.005.ix

    Article  PubMed  Google Scholar 

  20. B. Sacconi, R. Argiro, D. Diacinti, A. Iannarelli, M. Bezzi, C. Cipriani, D. Pisani, V. Cipolla, C. De Felice, S. Minisola, C. Catalano, MR appearance of parathyroid adenomas at 3 T in patients with primary hyperparathyroidism: what radiologists need to know for pre-operative localization. Eur. Radiol. 26(3), 664–673 (2016). doi:10.1007/s00330-015-3854-5

    Article  CAS  PubMed  Google Scholar 

  21. J.L. Chazen, A. Gupta, A. Dunning, C.D. Phillips, Diagnostic accuracy of 4D-CT for parathyroid adenomas and hyperplasia. AJNR. Am. J. Neuroradiol. 33(3), 429–433 (2012). doi:10.3174/ajnr.A2805

    Article  CAS  PubMed  Google Scholar 

  22. D.I. Kutler, R. Moquete, E. Kazam, W.I. Kuhel, Parathyroid localization with modified 4D-computed tomography and ultrasonography for patients with primary hyperparathyroidism. Laryngoscope 121(6), 1219–1224 (2011). doi:10.1002/lary.21783

    Article  PubMed  Google Scholar 

  23. M.M. Mortenson, D.B. Evans, J.E. Lee, G.J. Hunter, D. Shellingerhout, T. Vu, B.S. Edeiken, L. Feng, N.D. Perrier, Parathyroid exploration in the reoperative neck: improved preoperative localization with 4D-computed tomography. J. Am. Coll. Surg. 206(5), 888–895 (2008). doi:10.1016/j.jamcollsurg.2007.12.044. discussion 895-886

    Article  PubMed  Google Scholar 

  24. M.L. De Feo, S. Colagrande, C. Biagini, A. Tonarelli, G. Bisi, L. Vaggelli, D. Borrelli, P. Cicchi, F. Tonelli, A. Amorosi, M. Serio, M.L. Brandi, Parathyroid glands: combination of (99m)Tc MIBI scintigraphy and US for demonstration of parathyroid glands and nodules. Radiology 214(2), 393–402 (2000). doi:10.1148/radiology.214.2.r00fe04393

    Article  PubMed  Google Scholar 

  25. P.K. Leupe, P.R. Delaere, V.L. Vander Poorten, F. Debruyne, Pre-operative imaging in primary hyperparathyroidism with ultrasonography and sestamibi scintigraphy. B-ENT. 7(3), 173–180 (2011)

    CAS  PubMed  Google Scholar 

  26. S. Mazzeo, D. Caramella, R. Lencioni, N. Molea, A. De Liperi, C. Marcocci, P. Miccoli, P. Iacconi, G.B. Bossio, P. Viacava, E. Lazzeri, C. Bartolozzi, Comparison among sonography, double-tracer subtraction scintigraphy, and double-phase scintigraphy in the detection of parathyroid lesions. AJR. Am. J. Roentgenol. 166(6), 1465–1470 (1996). doi:10.2214/ajr.166.6.8633466

    Article  CAS  PubMed  Google Scholar 

  27. M.J. Lane, T.S. Desser, R.J. Weigel, R.B. Jeffrey Jr., Use of color and power Doppler sonography to identify feeding arteries associated with parathyroid adenomas. AJR. Am. J. Roentgenol. 171(3), 819–823 (1998). doi:10.2214/ajr.171.3.9725323

    Article  CAS  PubMed  Google Scholar 

  28. M. Dighe, U. Bae, M.L. Richardson, T.J. Dubinsky, S. Minoshima, Y. Kim, Differential diagnosis of thyroid nodules with US elastography using carotid artery pulsation. Radiology 248(2), 662–669 (2008). doi:10.1148/radiol.2482071758

    Article  PubMed  Google Scholar 

  29. S.H. Park, S.J. Kim, E.K. Kim, M.J. Kim, E.J. Son, J.Y. Kwak, Interobserver agreement in assessing the sonographic and elastographic features of malignant thyroid nodules. AJR. Am. J. Roentgenol. 193(5), W416–423 (2009). doi:10.2214/AJR.09.2541

    Article  PubMed  Google Scholar 

  30. P.V. Lippolis, S. Tognini, G. Materazzi, A. Polini, R. Mancini, C.E. Ambrosini, A. Dardano, F. Basolo, M. Seccia, P. Miccoli, F. Monzani, Is elastography actually useful in the presurgical selection of thyroid nodules with indeterminate cytology? J. Clin. Endocrinol. Metab. 96(11), E1826–1830 (2011). doi:10.1210/jc.2011-1021

    Article  CAS  PubMed  Google Scholar 

  31. F. Sebag, J. Vaillant-Lombard, J. Berbis, V. Griset, J.F. Henry, P. Petit, C. Oliver, Shear wave elastography: a new ultrasound imaging mode for the differential diagnosis of benign and malignant thyroid nodules. J. Clin. Endocrinol. Metab. 95(12), 5281–5288 (2010). doi:10.1210/jc.2010-0766

    Article  CAS  PubMed  Google Scholar 

  32. F. Magri, S. Chytiris, V. Capelli, S. Alessi, E. Nalon, M. Rotondi, S. Cassibba, F. Calliada, L. Chiovato, Shear wave elastography in the diagnosis of thyroid nodules: feasibility in the case of coexistent chronic autoimmune Hashimoto’s thyroiditis. Clin. Endocrinol. (Oxf). 76(1), 137–141 (2012). doi:10.1111/j.1365-2265.2011.04170.x

    Article  PubMed  Google Scholar 

  33. K.S. Bhatia, C.S. Tong, C.C. Cho, E.H. Yuen, Y.Y. Lee, A.T. Ahuja, Shear wave elastography of thyroid nodules in routine clinical practice: preliminary observations and utility for detecting malignancy. Eur. Radiol. 22(11), 2397–2406 (2012). doi:10.1007/s00330-012-2495-1

    Article  PubMed  Google Scholar 

  34. A. Agha, M. Hornung, C. Stroszczynski, H.J. Schlitt, E.M. Jung, Highly efficient localization of pathological glands in primary hyperparathyroidism using contrast-enhanced ultrasonography (CEUS) in comparison with conventional ultrasonography. J. Clin. Endocrinol. Metab. 98(5), 2019–2025 (2013). doi:10.1210/jc.2013-1007

    Article  CAS  PubMed  Google Scholar 

  35. G. Azizi, K. Piper, J.M. Keller, M.L. Mayo, D. Puett, K.M. Earp, C.D. Malchoff, Shear wave elastography and parathyroid adenoma: A new tool for diagnosing parathyroid adenomas. Eur. J. Radiol. 85(9), 1586–1593 (2016). doi:10.1016/j.ejrad.2016.06.009

    Article  PubMed  Google Scholar 

  36. A. Batur, M. Atmaca, A. Yavuz, M. Ozgokce, A. Bora, M.D. Bulut, H. Arslan, O. Toktas, M. Alpaslan, Ultrasound elastography for distinction between parathyroid adenomas and thyroid nodules. J. Ultrasound Med. 35(6), 1277–1282 (2016). doi:10.7863/ultra.15.07043

    Article  PubMed  Google Scholar 

  37. W.B. Li, B. Zhang, Q.L. Zhu, Y.X. Jiang, J. Sun, M. Yang, J.C. Li, Comparison between thin-slice 3-D volumetric ultrasound and conventional ultrasound in the differentiation of benign and malignant Thyroid Lesions. Ultrasound Med Biol. 41(12), 3096–3101 (2015). doi:10.1016/j.ultrasmedbio.2015.06.022

    Article  PubMed  Google Scholar 

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Authors and Affiliations

  1. Department of Experimental Medicine Sapienza University of Rome, Rome, Italy

    Andrea M. Isidori, Elisa Giannetta, Emilia Sbardella & Daniele Gianfrilli

  2. Department of Radiological, Oncological and Anatomo-Pathological Sciences, Sapienza University of Rome, Rome, Italy

    Vito Cantisani, Daniele Diacinti, Valerio Forte, Daniela Elia, Francesco Monteleone, Carlo Catalano & Ferdinando D’Ambrosio

  3. Department of Biomedical Sciences and Morphologic and Functional Imaging, Policlinico “G. Martino”, University of Messina, Messina, Italy

    Emanuele David & Giorgio Ascenti

  4. Department of Public Health and Infectious Diseases, Sapienza University of Rome, Rome, Italy

    Corrado De Vito

  5. Department of Internal Medicine and Medical Disciplines Sapienza University of Rome, Rome, Italy

    Jessica Pepe & Salvatore Minisola

  6. Department of Surgical Sciences, Sapienza University of Rome, Rome, Italy

    Vito D’Andrea

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  1. Andrea M. Isidori
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Andrea M. Isidori and Vito Cantisani equally contributed.

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Isidori, A.M., Cantisani, V., Giannetta, E. et al. Multiparametric ultrasonography and ultrasound elastography in the differentiation of parathyroid lesions from ectopic thyroid lesions or lymphadenopathies. Endocrine 57, 335–343 (2017). https://doi.org/10.1007/s12020-016-1116-1

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