Ultrasound Int Open 2017; 03(04): E137-E149
DOI: 10.1055/s-0043-119412
Review
© Georg Thieme Verlag KG Stuttgart · New York

Strain Elastography - How To Do It?

Christoph F. Dietrich
1   Caritas-Krankenhaus, Innere Medizin 2, Bad Mergentheim, Germany
,
Richard G. Barr
2   Radiology, Northeastern Ohio Medical University, Rootstown, United States
,
André Farrokh
3   Department of Breast Imaging and Interventions, University Hospital Schleswig-Holstein Campus Kiel, Kiel, Germany
,
Manjiri Dighe
4   Department of Biology, University of Washington, Radiology, Seattle, United States
,
Michael Hocke
5   HELIOS Klinikum Meiningen, Internal Medicine II, Meiningen, Germany
,
Christian Jenssen
6   Krankenhaus Märkisch Oderland Strausberg/ Wriezen, Klinik für Innere Medizin, Wriezen, Germany
,
Yi Dong
7   Zhongshan Hospital, Ultrasound, Shanghai, China
,
Adrian Saftoiu
8   University of Medicine and Pharmacy of Craiova, Research Center of Gastroenterology and Hepatology, Craiova, Romania
,
Roald Flesland Havre
9   Department of Medicine, Haukeland University Hospital, Bergen, Norway
› Author Affiliations
Further Information

Publication History

received 28 May 2017
revised 27 August 2017

accepted 29 August 2017

Publication Date:
07 December 2017 (online)

Abstract

Tissue stiffness assessed by palpation for diagnosing pathology has been used for thousands of years. Ultrasound elastography has been developed more recently to display similar information on tissue stiffness as an image. There are two main types of ultrasound elastography, strain and shear wave. Strain elastography is a qualitative technique and provides information on the relative stiffness between one tissue and another. Shear wave elastography is a quantitative method and provides an estimated value of the tissue stiffness that can be expressed in either the shear wave speed through the tissues in meters/second, or converted to the Young’s modulus making some assumptions and expressed in kPa. Each technique has its advantages and disadvantages and they are often complimentary to each other in clinical practice. This article reviews the principles, technique, and interpretation of strain elastography in various organs. It describes how to optimize technique, while pitfalls and artifacts are also discussed.

 
  • References

  • 1 Dietrich CF et al. How to perform endoscopic ultrasoud elastography. Endosc Ultrasound 2017 in press
  • 2 Bamber J, Cosgrove D, Dietrich CF, Fromageau J, Bojunga J, Calliada F, Cantisani V. et al. EFSUMB guidelines and recommendations on the clinical use of ultrasound elastography. Part 1: Basic principles and technology. Ultraschall Med 2013; 34: 169-184
  • 3 Shiina T, Nightingale KR, Palmeri ML, Hall TJ, Bamber JC, Barr RG, Castera L. et al. WFUMB guidelines and recommendations for clinical use of ultrasound elastography: Part 1: basic principles and terminology. Ultrasound Med Biol 2015; 41: 1126-1147
  • 4 Cosgrove D, Piscaglia F, Bamber J, Bojunga J, Correas JM, Gilja OH, Klauser AS. et al. EFSUMB guidelines and recommendations on the clinical use of ultrasound elastography. Part 2: Clinical applications. Ultraschall Med 2013; 34: 238-253
  • 5 Ferraioli G, Filice C, Castera L, Choi BI, Sporea I, Wilson SR, Cosgrove D. et al. WFUMB guidelines and recommendations for clinical use of ultrasound elastography: Part 3: liver. Ultrasound Med Biol 2015; 41: 1161-1179
  • 6 Dong Y, Sirli R, Ferraioli G, Sporea I, Chiorean L, Cui X, Fan M. et al. Shear wave elastography of the liver - review on normal values. Z Gastroenterol 2017; 55: 153-166
  • 7 Dietrich CF, Bamber J, Berzigotti A, Bota S, Cantisani V, Castera L, Cosgrove D. et al. EFSUMB Guidelines and recommendations on the clinical use of liver ultrasound elastography, Update 2017 (Long Version). Ultraschall Med 2017; 38: e16-e47
  • 8 Dietrich CF, Bamber J, Berzigotti A, Bota S, Cantisani V, Castera L, Cosgrove D. et al. EFSUMB Guidelines and recommendations on the clinical use of liver ultrasound elastography, Update 2017 (Short Version). Ultraschall Med 2017; 38: 377-394
  • 9 Cui XW, Friedrich-Rust M, De Molo C, Ignee A, Schreiber-Dietrich D, Dietrich CF. Liver elastography, comments on EFSUMB elastography guidelines 2013. World J Gastroenterol 2013; 19: 6329-6347
  • 10 Barr RG, Zhang Z. Effects of precompression on elasticity imaging of the breast: development of a clinically useful semiquantitative method of precompression assessment. J Ultrasound Med 2012; 31: 895-902
  • 11 Bilgen M, Insana MF. Error analysis in acoustic elastography. II. Strain estimation and SNR analysis. J Acoust Soc Am 1997; 101: 1147-1154
  • 12 Havre RF, Elde E, Gilja OH, Odegaard S, Eide GE, Matre K, Nesje LB. Freehand real-time elastography: impact of scanning parameters on image quality and in vitro intra- and interobserver validations. Ultrasound Med Biol 2008; 34: 1638-1650
  • 13 Itoh A, Ueno E, Tohno E, Kamma H, Takahashi H, Shiina T, Yamakawa M. et al. Breast disease: clinical application of US elastography for diagnosis. Radiology 2006; 239: 341-350
  • 14 Cho N, Moon WK, Chang JM, Kim SJ, Lyou CY, Choi HY. Aliasing artifact depicted on ultrasound (US)-elastography for breast cystic lesions mimicking solid masses. Acta Radiol 2011; 52: 3-7
  • 15 Barr RG, Lackey AE. The utility of the "bull's-eye" artifact on breast elasticity imaging in reducing breast lesion biopsy rate. Ultrasound Q 2011; 27: 151-155
  • 16 Pallwein L, Mitterberger M, Struve P, Pinggera G, Horninger W, Bartsch G, Aigner F. et al. Real-time elastography for detecting prostate cancer: preliminary experience. BJU Int 2007; 100: 42-46
  • 17 Pallwein L, Aigner F, Faschingbauer R, Pallwein E, Pinggera G, Bartsch G, Schaefer G. et al. Prostate cancer diagnosis: value of real-time elastography. Abdom Imaging 2008; 33: 729-735
  • 18 Aigner F, Pallwein L, Junker D, Schafer G, Mikuz G, Pedross F, Mitterberger MJ. et al. Value of real-time elastography targeted biopsy for prostate cancer detection in men with prostate specific antigen 1.25 ng/ml or greater and 4.00 ng/ml or less. J Urol 2010; 184: 913-917
  • 19 Aigner F, Pallwein L, Schocke M, Lebovici A, Junker D, Schafer G, Mikuz G. et al. Comparison of real-time sonoelastography with T2-weighted endorectal magnetic resonance imaging for prostate cancer detection. J Ultrasound Med 2011; 30: 643-649
  • 20 Barr RG, Nakashima K, Amy D, Cosgrove D, Farrokh A, Schafer F, Bamber JC. et al. WFUMB guidelines and recommendations for clinical use of ultrasound elastography: Part 2: breast. Ultrasound Med Biol 2015; 41: 1148-1160
  • 21 Friedrich-Rust M, Vorlaender C, Dietrich CF, Kratzer W, Blank W, Schuler A, Broja N. et al. Evaluation of strain elastography for differentiation of thyroid nodules: Results of a prospective DEGUM multicenter study. Ultraschall Med 2016; 37: 262-270
  • 22 Dietrich CF, Bojunga J. Ultrasound of the thyroid. Z Gastroenterol 2015; 53: 208-225
  • 23 Cosgrove D, Barr R, Bojunga J, Cantisani V, Chammas MC, Dighe M, Vinayak S et al. WFUMB Guidelines and recommendations on the clinical use of ultrasound elastography: Part 4. Thyroid. Ultrasound Med Biol 2016
  • 24 Chiorean L, Barr RG, Braden B, Jenssen C, Cui XW, Hocke M, Schuler A. et al. Transcutaneous ultrasound: Elastographic lymph node evaluation. Current clinical applications and literature review. Ultrasound Med Biol 2016; 42: 16-30
  • 25 Havre RF, Leh SM, Gilja OH, Odegaard S, Waage JE, Baatrup G, Nesje LB. Differentiation of metastatic and non-metastatic mesenteric lymph nodes by strain elastography in surgical specimens. Ultraschall Med 2016
  • 26 Cui XW, Hocke M, Jenssen C, Ignee A, Klein S, Schreiber-Dietrich D, Dietrich CF. Conventional ultrasound for lymph node evaluation, update 2013. Z Gastroenterol 2014; 52: 212-221
  • 27 Cui XW, Jenssen C, Saftoiu A, Ignee A, Dietrich CF. New ultrasound techniques for lymph node evaluation. World J Gastroenterol 2013; 19: 4850-4860
  • 28 Dietrich CF, Hocke M, Jenssen C. Ultrasound for abdominal lymphadenopathy. Dtsch Med Wochenschr 2013; 138: 1001-1018
  • 29 Dietrich CF, Ponnudurai R, Bachmann Nielsen M. Is there a need for new imaging methods for lymph node evaluation?. Ultraschall Med 2012; 33: 411-414
  • 30 Dietrich CF. Echtzeit-Gewebeelastographie. Anwendungsmöglichkeiten nicht nur im Gastrointestinaltrakt. Endheu 2010; 23: 177-225
  • 31 Dietrich CF. Multiple clinical applications. Multiple clinical solutions. Endheu 2012; 24: 177-225
  • 32 Dietrich CF, Hirche TO, Ott M, Ignee A. Real-time tissue elastography in the diagnosis of autoimmune pancreatitis. Endoscopy 2009; 41: 718-720
  • 33 Hirche TO, Ignee A, Barreiros AP, Schreiber-Dietrich D, Jungblut S, Ott M, Hirche H. et al. Indications and limitations of endoscopic ultrasound elastography for evaluation of focal pancreatic lesions. Endoscopy 2008; 40: 910-917
  • 34 Saftoiu A, Vilmann P, Gorunescu F, Janssen J, Hocke M, Larsen M, Iglesias-Garcia J. et al. Efficacy of an artificial neural network-based approach to endoscopic ultrasound elastography in diagnosis of focal pancreatic masses. Clin Gastroenterol Hepatol 2012; 10: 84-90 e81
  • 35 Saftoiu A, Vilmann P, Gorunescu F, Janssen J, Hocke M, Larsen M, Iglesias-Garcia J. et al. Accuracy of endoscopic ultrasound elastography used for differential diagnosis of focal pancreatic masses: A multicenter study. Endoscopy 2011; 43: 596-603
  • 36 Havre RF, Odegaard S, Gilja OH, Nesje LB. Characterization of solid focal pancreatic lesions using endoscopic ultrasonography with real-time elastography. Scand J Gastroenterol 2014; 49: 742-751
  • 37 Cui XW, Chang JM, Kan QC, Chiorean L, Ignee A, Dietrich CF. Endoscopic ultrasound elastography: Current status and future perspectives. World J Gastroenterol 2015; 21: 13212-13224
  • 38 Dietrich CF, Saftoiu A, Jenssen C. Real time elastography endoscopic ultrasound (RTE-EUS), a comprehensive review. Eur J Radiol 2014; 83: 405-414
  • 39 Janssen J, Dietrich CF, Will U, Greiner L. Endosonographic elastography in the diagnosis of mediastinal lymph nodes. Endoscopy 2007; 39: 952-957
  • 40 Dietrich CF, Jenssen C, Hocke M, Cui XW, Woenckhaus M, Ignee A. Imaging of gastrointestinal stromal tumours with modern ultrasound techniques – a pictorial essay. Z Gastroenterol 2012; 50: 457-467
  • 41 Waage JE, Bach SP, Pfeffer F, Leh S, Havre RF, Odegaard S, Baatrup G. Combined endorectal ultrasonography and strain elastography for the staging of early rectal cancer. Colorectal Dis 2015; 17: 50-56
  • 42 Waage JE, Havre RF, Odegaard S, Leh S, Eide GE, Baatrup G. Endorectal elastography in the evaluation of rectal tumours. Colorectal Dis 2011; 13: 1130-1137
  • 43 Waage JE, Leh S, Rosler C, Pfeffer F, Bach SP, Havre RF, Haldorsen IS. et al. Endorectal ultrasonography, strain elastography and MRI differentiation of rectal adenomas and adenocarcinomas. Colorectal Dis 2015; 17: 124-131
  • 44 Waage JE, Rafaelsen SR, Borley NR, Havre RF, Gubberud ET, Leh S, Kolbro T. et al. Strain elastography evaluation of rectal tumors: inter- and intraobserver reproducibility. Ultraschall Med 2015; 36: 611-617
  • 45 Allgayer H, Ignee A, Dietrich CF. Endosonographic elastography of the anal sphincter in patients with fecal incontinence. Scand J Gastroenterol 2010; 45: 30-38
  • 46 Allgayer H, Ignee A, Zipse S, Crispin A, Dietrich CF. Endorectal ultrasound and real-time elastography in patients with fecal incontinence following anorectal surgery: A prospective comparison evaluating short- and long-term outcomes in irradiated and non-irradiated patients. Z Gastroenterol 2012; 50: 1281-1286
  • 47 Havre R, Gilja OH. Elastography and strain rate imaging of the gastrointestinal tract. Eur J Radiol 2014; 83: 438-441
  • 48 Havre RF, Leh S, Gilja OH, Odegaard S, Waage JE, Baatrup G, Nesje LB. Strain assessment in surgically resected inflammatory and neoplastic bowel lesions. Ultraschall Med 2014; 35: 149-158
  • 49 Barr RG, Cosgrove D, Brock M, Cantisani V, Correas JM, Postema AW, Salomon G et al. WFUMB Guidelines and recommendations on the clinical use of ultrasound elastography: Part 5. Prostate. Ultrasound Med Biol 2016
  • 50 Wojcinski S, Boehme E, Farrokh A, Soergel P, Degenhardt F, Hillemanns P. Ultrasound real-time elastography can predict malignancy in BI-RADS(R)-US 3 lesions. BMC Cancer 2013; 13: 159
  • 51 Farrokh A, Wojcinski S, Degenhardt F. Diagnostic value of strain ratio measurement in the differentiation of malignant and benign breast lesions. Ultraschall Med 2011; 32: 400-405
  • 52 Sadigh G, Carlos RC, Neal CH, Dwamena BA. Accuracy of quantitative ultrasound elastography for differentiation of malignant and benign breast abnormalities: a meta-analysis. Breast Cancer Res Treat 2012; 134: 923-931
  • 53 Dighe M, Bae U, Richardson ML, Dubinsky TJ, Minoshima S, Kim Y. Differential diagnosis of thyroid nodules with US elastography using carotid artery pulsation. Radiology 2008; 248: 662-669
  • 54 Friedrich-Rust M, Sperber A, Holzer K, Diener J, Grunwald F, Badenhoop K, Weber S. et al. Real-time elastography and contrast-enhanced ultrasound for the assessment of thyroid nodules. Exp Clin Endocrinol Diabetes 2010; 118: 602-609
  • 55 Havre RF, Waage JR, Gilja OH, Odegaard S, Nesje LB.Real-Time elastography strain ratio measurements are influenced by the position of the reference area. Ultraschall Med. 2012; 33: 559–568
  • 56 Barr RG, Destounis S, Lackey 2nd LB, Svensson WE, Balleyguier C, Smith C. Evaluation of breast lesions using sonographic elasticity imaging: A multicenter trial. J Ultrasound Med 2012; 31: 281-287
  • 57 Barr RG, Zhang Z. Shear-wave elastography of the breast: value of a quality measure and comparison with strain elastography. Radiology 2015; 275: 45-53
  • 58 Grajo JR, Barr RG. Strain elastography for prediction of breast cancer tumor grades. J Ultrasound Med 2014; 33: 129-134
  • 59 Koehler KE, Ohlinger R. Sensitivity and specificity of preoperative ultrasonography for diagnosing nodal metastases in patients with breast cancer. Ultraschall Med 2011; 32: 393-399
  • 60 Wojcinski S, Dupont J, Schmidt W, Cassel M, Hillemanns P. Real-time ultrasound elastography in 180 axillary lymph nodes: Elasticity distribution in healthy lymph nodes and prediction of breast cancer metastases. BMC Med Imaging 2012; 12: 35
  • 61 Park YM, Fornage BD, Benveniste AP, Fox PS, Bassett Jr. RL, Yang WT. Strain elastography of abnormal axillary nodes in breast cancer patients does not improve diagnostic accuracy compared with conventional ultrasound alone. AJR Am J Roentgenol 2014; 203: 1371-1378
  • 62 Cosgrove D, Barr R, Bojunga J, Cantisani V, Chammas MC, Dighe M, Vinayak S. et al. WFUMB Guidelines and Recommendations on the Clinical Use of Ultrasound Elastography: Part 4. Thyroid. Ultrasound Med Biol 2017; 43: 4-26
  • 63 Dighe M, Barr R, Bojunga J, Cantisani V, Chammas MC, Cosgrove D, Cui XW. et al. Thyroid Ultrasound: State of the Art Part 1 – Thyroid Ultrasound reporting and Diffuse Thyroid Diseases. Med Ultrason 2017; 19: 79-93
  • 64 Wang Y, Dan HJ, Dan HY, Li T, Hu B. Differential diagnosis of small single solid thyroid nodules using real-time ultrasound elastography. J Int Med Res 2010; 38: 466-472
  • 65 Tranquart F, Bleuzen A, Pierre-Renoult P, Chabrolle C, Sam Giao M, Lecomte P. Elastosonography of thyroid lesions. J Radiol 2008; 89: 35-39
  • 66 Shuzhen C. Comparison analysis between conventional ultrasonography and ultrasound elastography of thyroid nodules. Eur J Radiol 2012; 81: 1806-1811
  • 67 Rago T, Vitti P. Role of thyroid ultrasound in the diagnostic evaluation of thyroid nodules. Best Pract Res Clin Endocrinol Metab 2008; 22: 913-928
  • 68 Rago T, Di Coscio G, Basolo F, Scutari M, Elisei R, Berti P, Miccoli P. et al. Combined clinical, thyroid ultrasound and cytological features help to predict thyroid malignancy in follicular and Hupsilonrthle cell thyroid lesions: results from a series of 505 consecutive patients. Clin Endocrinol (Oxf) 2007; 66: 13-20
  • 69 Asteria C, Giovanardi A, Pizzocaro A, Cozzaglio L, Morabito A, Somalvico F, Zoppo A. US-elastography in the differential diagnosis of benign and malignant thyroid nodules. Thyroid 2008; 18: 523-531
  • 70 Ciledag N, Arda K, Aribas BK, Aktas E, Köse SK. The utility of ultrasound elastography and MicroPure imaging in the differentiation of benign and malignant thyroid nodules. AJR Am J Roentgenol 2012; 198: W244-W249
  • 71 Aydin R, Elmali M, Polat AV, Danaci M, Akpolat I. Comparison of muscle-to-nodule and parenchyma-to-nodule strain ratios in the differentiation of benign and malignant thyroid nodules: Which one should we use?. Eur J Radiol 2014; 83: e131-E136
  • 72 Cantisani V, Grazhdani H, Drakonaki E et al. HYPERLINK "https://www.ncbi.nlm.nih.gov/pubmed/25954310" Strain US Elastography for the Characterization of Thyroid Nodules: Advantages and Limitation. Int J Endocrinol 2015; doi: 10.1155/2015/908575
  • 73 Cantisani V, Lodise P, Grazhdani H. et al. HYPERLINK "https://www.ncbi.nlm.nih.gov/pubmed/23763859" Ultrasound elastography in the evaluation of thyroid pathology. Current status. Eur J Radiol 2014; 83: 420-428. doi: 10.1016/j.ejrad.2013.05.008
  • 74 Ding J, Cheng H, Ning C, Huang J, Zhang Y. Quantitative measurement for thyroid cancer characterization based on elastography. J Ultrasound Med 2011; 30: 1259-1266
  • 75 Xing P, Wu L, Zhang C, Li S, Liu C, Wu C. Differentiation of benign from malignant thyroid lesions: Calculation of the strain ratio on thyroid sonoelastography. J Ultrasound Med 2011; 30: 663-669
  • 76 Kagoya R, Monobe H, Tojima H. Utility of elastography for differential diagnosis of benign and malignant thyroid nodules. Otolaryngol Head Neck Surg 2010; 143: 230-234
  • 77 Cantisani V, Maceroni P, D'Andrea V, Patrizi G, Di Segni M, De Vito C, Grazhdani H. et al. Strain ratio ultrasound elastography increases the accuracy of colour-Doppler ultrasound in the evaluation of Thy-3 nodules. A bi-centre university experience. Eur Radiol 2016; 26: 1441-1449
  • 78 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 Med 2015; 36: 162-167 doi: 10.1055/s-0034-1366467
  • 79 Xue J, Cao XL, Shi L, Lin CH, Wang J, Wang L. The diagnostic value of combination of TI-RADS and ultrasound elastography in the differentiation of benign and malignant thyroid nodules. Clin Imaging 2016; 40: 913-916
  • 80 Barr RG, Cosgrove D, Brock M, Cantisani V, Correas JM, Postema AW, Salomon G. et al. WFUMB Guidelines and recommendations on the clinical use of ultrasound elastography: Part 5. Prostate. Ultrasound Med Biol 2017; 43: 27-48
  • 81 Kamoi K, Okihara K, Ochiai A, Ukimura O, Mizutani Y, Kawauchi A, Miki T. The utility of transrectal real-time elastography in the diagnosis of prostate cancer. Ultrasound Med Biol 2008; 34: 1025-1032
  • 82 Xu G, Feng L, Yao M, Wu J, Guo L, Yao X, Zhao L. et al. A new 5-grading score in the diagnosis of prostate cancer with real-time elastography. Int J Clin Exp Pathol 2014; 7: 4128-4135
  • 83 Fujimoto K, Kato M, Kudo M, Yada N, Shiina T, Ueshima K, Yamada Y. et al. Novel image analysis method using ultrasound elastography for noninvasive evaluation of hepatic fibrosis in patients with chronic hepatitis C. Oncology 2013; 84 (Suppl. 01) 3-12
  • 84 Tatsumi C, Kudo M, Ueshima K, Kitai S, Ishikawa E, Yada N, Hagiwara S. et al. Non-invasive evaluation of hepatic fibrosis for type C chronic hepatitis. Intervirology 2010; 53: 76-81
  • 85 Friedrich-Rust M, Wunder K, Kriener S, Sotoudeh F, Richter S, Bojunga J, Herrmann E. et al. Liver fibrosis in viral hepatitis: noninvasive assessment with acoustic radiation force impulse imaging versus transient elastography. Radiology 2009; 252: 595-604