Ultraschall Med 2016; 37(03): 262-270
DOI: 10.1055/s-0042-104647
Original Article
© Georg Thieme Verlag KG Stuttgart · New York

Evaluation of Strain Elastography for Differentiation of Thyroid Nodules: Results of a Prospective DEGUM Multicenter Study

Evaluation der Strain Elastografie für die Differenzierung von Schilddrüsenknoten: Ergebnisse einer prospektiven DEGUM Multizenter-Studie
M. Friedrich-Rust*
1   Department of Internal Medicine 1, J.W. Goethe-University Hospital, Frankfurt, Germany
,
C. Vorlaender*
2   Department of General Surgery, Buergerhospital Frankfurt, Germany
,
C. F. Dietrich
3   Innere Medizin 2, Caritas Hospital, Bad Mergentheim, Germany
,
W. Kratzer
4   Department of Internal Medicine I, University Hospital Ulm, Germany
,
W. Blank
5   Medizinische Klinik 1, Hospital am Steinenberg, Reutlingen, Germany
,
A. Schuler
6   Department of Internal Medicine, Helfenstein Hospital, Geislingen, Germany
,
N. Broja
1   Department of Internal Medicine 1, J.W. Goethe-University Hospital, Frankfurt, Germany
,
X. W. Cui
3   Innere Medizin 2, Caritas Hospital, Bad Mergentheim, Germany
7   Sino-German Research Center of Ultrasound in Medicine, The First Affiliated Hospital of Zhengzhou University, Zhengzhou, China
,
E. Herrmann
8   Institute of Biostatistics and Mathematical Modelling, Faculty of Medicine, J.W. Goethe-University, Frankfurt, Germany
,
J. Bojunga
1   Department of Internal Medicine 1, J.W. Goethe-University Hospital, Frankfurt, Germany
› Author Affiliations
Further Information

Publication History

30 October 2015

22 February 2016

Publication Date:
12 April 2016 (online)

Abstract

Purpose: Many patients with thyroid nodules are presently referred to surgery for not only therapeutic but also diagnostic purposes. The aim of noninvasive diagnostic methods is to optimize the selection of patients for surgery. Strain elastography (SE) enables the ultrasound-based determination of tissue elasticity. The aim of the present study was to evaluate the value of SE for the differentiation of thyroid nodules in a prospective multicenter study.

Materials and Methods: The study was registered at clinicaltrials.gov and was approved by the local ethics committees of all participating centers. All patients received an ultrasound (US) of the thyroid gland including color Doppler US. In addition, all nodules were evaluated by SE (Hitachi Medical Systems) using qualitative image interpretation of color distribution (SE-ES), strain value and strain ratio.

Results: Overall, 602 patients with 657 thyroid nodules (567 benign, 90 malignant) from 7 centers were included in the final analysis. The sensitivity, specificity, NPV, PPV, +LR were 21 %, 73 %, 86 %, 11 %, 0.8, respectively, for color Doppler US; 69 %, 75 %, 94 %, 30 %, 2.9, respectively, for SE-ES; 56 %, 81 %, 92 %, 32 %, 2.9, respectively, for SE-strain value; and 58 %, 78 %, 92 %, 30 %, 2.6, respectively, for SE-strain ratio. The diagnostic accuracy was 71 % for both strain value and strain ratio of nodules.

Conclusion: SE as an additional ultrasound tool improves the value of ultrasound for the work-up of thyroid nodules. It might reduce diagnostic surgery of thyroid nodules in the future.

Zusammenfassung

Ziel: Viele Patienten mit Schilddrüsenknoten werden nicht nur therapeutisch, sondern auch zu diagnostischem Zweck operiert. Ziel von nicht-invasiven diagnostischen Verfahren ist es daher die Selektion von Patienten zur Operation zu optimieren. Strain Elastografie (SE) ermöglicht die Ultraschall-basierte Messung der Gewebeelastizität. Das Ziel der vorliegenden Studie war es den Stellenwert der SE in einer prospektiven Multizenter-Studie für die Differenzierung von Schilddrüsenknoten zu evaluieren.

Material und Methoden: Die Studie wurde bei clinicaltrials.gov registriert und von den lokalen Ethikkommissionen der teilnehmenden Zentren genehmigt. Alle Patienten erhielten einen Ultraschall (US) der Schilddrüse inklusive Farbduplex-US. Zusätzlich wurden alle Knoten mittels SE (Hitachi Medical System) untersucht und eine Beurteilung der qualitativen Farbverteilung (SE-ES) und eine semiquantitative Messung der Elastizität mittels strain value und strain ratio durchgeführt.

Ergebnisse: Insgesamt wurden 602 Patienten mit 657 Schilddrüsenknoten (567 benigne, 90 maligne) an 7 deutschen Zentren ausgewertet. Sensitivität, Spezifität, NPV, PPV, und +LR betrugen entsprechend 21 %, 73 %, 86 %, 11 %, 0,8 für den Duplex-US; 69 %, 75 %, 94 %, 30 %, 2,9 für SE-ES; 56 %, 81 %, 92 %, 32 %, 2,9 für SE-strain value; 58 %, 78 %, 92 %, 30 %, 2,6 für SE- strain ratio. Die diagnostische Genauigkeit betrug 71 % sowohl für SE-strain value, als auch SE-strain ratio.

Schlussfolgerung: Strain Elastografie als zusätzliche Ultraschallfunktion verbessert die Ultraschall-Diagnostik von Schilddrüsenknoten und könnte in Zukunft die Zahl der diagnostischen Operationen von Schilddrüsenknoten reduzieren.

* both authors contributed equally


Tabelle 1a + b/Table 1a + b

 
  • References

  • 1 Reiners C, Wegscheider K, Schicha H et al. Prevalence of thyroid disorders in the working population of Germany: ultrasonography screening in 96278 unselected employees. Thyroid [Internet] 2004; 14: 926-932
  • 2 Iannuccilli JD, Cronan JJ, Monchik JM. Risk for malignancy of thyroid nodules as assessed by sonographic criteria: the need for biopsy. J Ultrasound Med 2004; 23: 1455-1464
  • 3 Cooper DS, Doherty GM, Haugen BR et al. Management guidelines for patients with thyroid nodules and differentiated thyroid cancer. Thyroid 2006; 16: 109-142
  • 4 Dietlein M, Schicha H. Lifetime follow-up care is necessary for all patients with treated thyroid nodules. Eur J Endocrinol 2003; 148: 377-379
  • 5 Gharib H, Papini E, Paschke R et al. American Association of Clinical Endocrinologists, Associazione Medici Endocrinologi, and EuropeanThyroid Association Medical Guidelines for Clinical Practice for the Diagnosis and Management of Thyroid Nodules. Endocr Pract 2010; 16 (Suppl. 01) 1-43
  • 6 Hegedus L. Clinical practice. The thyroid nodule. N Engl J Med 2004; 351: 1764-1771
  • 7 Haugen BR, Alexander EK, Bible KC et al. 2015 American Thyroid Association Management Guidelines for Adult Patients with Thyroid Nodules and Differentiated Thyroid Cancer. Thyroid [Internet] 2015; Available from: 20 http://www.ncbi.nlm.nih.gov/pubmed/26462967
  • 8 La Rosa GL, Belfiore A, Giuffrida D et al. Evaluation of the fine needle aspiration biopsy in the preoperative selection of cold thyroid nodules. Cancer 1991; 67: 2137-2141
  • 9 Oertel YC, Miyahara-Felipe L, Mendoza MG et al. Value of repeated fine needle aspirations of the thyroid: an analysis of over ten thousand FNAs. Thyroid 2007; 17: 1061-1066
  • 10 Peng Y, Wang HH. A meta-analysis of comparing fine-needle aspiration and frozen section for evaluating thyroid nodules. Diagn Cytopathol 2008; 36: 916-920
  • 11 Tee YY, Lowe AJ, Brand CA et al. Fine-needle aspiration may miss a third of all malignancy in palpable thyroid nodules: a comprehensive literature review. Ann Surg 2007; 246: 714-720
  • 12 Wienhold R, Scholz M, Adler JB et al. The management of thyroid nodules—a retrospective analysis of health insurance data. Dtsch Arztebl Int 2013; 110: 827-834
  • 13 Pacini F, Schlumberger M, Dralle H et al. European consensus for the management of patients with differentiated thyroid carcinoma of the follicular epithelium. Eur J Endocrinol 2006; 154: 787-803
  • 14 Bamber J, Cosgrove D, Dietrich CF et al. EFSUMB guidelines and recommendations on the clinical use of ultrasound elastography. Part 1: Basic principles and technology. Ultraschall in Med 2013; 34: 169-184
  • 15 Cosgrove D, Piscaglia F, Bamber J et al. EFSUMB guidelines and recommendations on the clinical use of ultrasound elastography. Part 2: Clinical applications. Ultraschall in Med 2013; 34: 238-253
  • 16 Bojunga J, Herrmann E, Meyer G et al. Realtime elastography for the differentiation of benign and malignant thyroid nodules: a meta-analysis. Thyroid 2010; 20: 1145-1150
  • 17 Ghajarzadeh M, Sodagari F, Shakiba M. Diagnostic accuracy of sonoelastography in detecting malignant thyroid nodules: a systematic review and meta-analysis. Am J Roentgenol 2014; 202: W379-W389
  • 18 Razavi SA, Hadduck TA, Sadigh G et al. Comparative effectiveness of elastographic and B-mode ultrasound criteria for diagnostic discrimination of thyroid nodules: a meta-analysis. Am J Roentgenol 2013; 200: 1317-1326
  • 19 Moon HJ, Sung JM, Kim EK et al. Diagnostic performance of gray-scale US and elastography in solid thyroid nodules. Radiology 2012; 262: 1002-1013
  • 20 Guidelines of the Papanicolaou Society of Cytopathology for the Examination of Fine-Needle Aspiration Specimens from Thyroid Nodules. The Papanicolaou Society of Cytopathology Task Force on Standards of Practice. Mod Pathol 1996; 9: 710-715
  • 21 Cibas ES, Ali SZ. The Bethesda System For Reporting Thyroid Cytopathology. Am J Clin Pathol 2009; 132: 658-665 Hospital
  • 22 Ivanac G, Brkljacic B, Ivanac K et al. Vascularisation of benign and malignant thyroid nodules: CD US evaluation. Ultraschall in Med 2007; 28: 502-506
  • 23 Ophir J, Cespedes I, Ponnekanti H et al. Elastography: a quantitative method for imaging the elasticity of biological tissues. Ultrason Imaging 1991; 13: 111-134
  • 24 Frey H. Realtime-elastography. A new ultrasound procedure for the reconstruction of tissue elasticity. Radiologe 2003; 43: 850-855
  • 25 Asteria C, Giovanardi A, Pizzocaro A et al. US-elastography in the differential diagnosis of benign and malignant thyroid nodules. Thyroid 2008; 18: 523-531
  • 26 Rubaltelli L, Corradin S, Dorigo A et al. Differential diagnosis of benign and malignant thyroid nodules at elastosonography. Ultraschall in Med 2009; 30: 175-179
  • 27 Friedrich-Rust M, Sperber A, Holzer K et al. Real-time Elastography and Contrast-Enhanced Ultrasound for the Assessment of Thyroid Nodules. Exp Clin Endocrinol Diabetes 2010; 118: 602-609
  • 28 Robin X, Turck N, Hainard A et al. pROC: an open-source package for R and S+ to analyze and compare ROC curves. BMC Bioinformatics 2011; 12: 77
  • 29 Ding J, Cheng H, Ning C et al. Quantitative measurement for thyroid cancer characterization based on elastography. J Ultrasound Med 2011; 30: 1259-1266
  • 30 Vorlander C, Wolff J, Saalabian S et al. Real-time ultrasound elastography--a noninvasive diagnostic procedure for evaluating dominant thyroid nodules. Langenbecks Arch Surg 2010; 395: 865-871
  • 31 Ning CP, Jiang SQ, Zhang T et al. The value of strain ratio in differential diagnosis of thyroid solid nodules. Eur J Radiol 2012; 81: 286-291
  • 32 Azizi G, Keller J, Lewis M et al. Performance of elastography for the evaluation of thyroid nodules: a prospective study. Thyroid 2013; 23: 734-740
  • 33 Magri F, Chytiris S, Capelli V et al. Comparison of elastographic strain index and thyroid fine-needle aspiration cytology in 631 thyroid nodules. J Clin Endocrinol Metab 2013; 98: 4790-4797
  • 34 Cantisani V, Lodise P, Di Rocco G et al. Diagnostic accuracy and interobserver agreement of Quasistatic Ultrasound Elastography in the diagnosis of thyroid nodules. Ultraschall in Med 2015; 36: 162-167
  • 35 Lippolis PV, Tognini S, Materazzi G et al. Is elastography actually useful in the presurgical selection of thyroid nodules with indeterminate cytology?. J Clin Endocrinol Metab 2011; 96: E1826-E1830
  • 36 Unluturk U, Erdogan MF, Demir O et al. Ultrasound elastography is not superior to grayscale ultrasound in predicting malignancy in thyroid nodules. Thyroid 2012; 22: 1031-1038
  • 37 Rubaltelli L, Corradin S, Dorigo A et al. Differential Diagnosis of Benign and Malignant Thyroid Nodules at Elastosonography. Ultraschall in Med 2009; 30: 175-179
  • 38 Hong Y, Liu X, Li Z et al. Real-time ultrasound elastography in the differential diagnosis of benign and malignant thyroid nodules. J Ultrasound Med 2009; 28: 861-867
  • 39 Lyshchik A, Higashi T, Asato R et al. Thyroid gland tumor diagnosis at US Elastography. Radiology 2005; 237: 202-211
  • 40 Rago T, Santini F, Scutari M et al. Elastography: new developments in ultrasound for predicting malignancy in thyroid nodules. J Clin Endocrinol Metab 2007; 92: 2917-2922
  • 41 Bojunga J, Dauth N, Berner C et al. Acoustic radiation force impulse imaging for differentiation of thyroid nodules. PLoS One 2012; 7: e42735
  • 42 Friedrich-Rust M, Meyer G, Dauth N et al. Interobserver agreement of Thyroid Imaging Reporting and Data System (TIRADS) and strain elastography for the assessment of thyroid nodules. PLoS One 2013; 8: e77927
  • 43 Trimboli P, Guglielmi R, Monti S et al. Ultrasound sensitivity for thyroid malignancy is increased by real-time elastography: a prospective multicenter study. J Clin Endocrinol Metab 2012; 97: 4524-4530
  • 44 Cantisani V, Grazhdani H, Ricci P et al. Q-elastosonography of solid thyroid nodules: assessment of diagnostic efficacy and interobserver variability in a large patient cohort. Eur Radiol 2014; 24: 143-150
  • 45 Lin P, Chen M, Liu B et al. Diagnostic performance of shear wave elastography in the identification of malignant thyroid nodules: a meta-analysis. Eur Radiol 2014; 24: 2729-2738
  • 46 Lyshchik A, Higashi T, Asato R et al. Thyroid gland tumor diagnosis at US elastography. Radiology 2005; 237: 202-211