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Elastography and strain rate imaging of the gastrointestinal tract
European Journal of Radiology 83 (2014) 438–441
Contents lists available at ScienceDirect
European Journal of Radiology journal homepage: www.elsevier.com/locate/ejrad
Elastography and strain rate imaging of the gastrointestinal tract R. Havre a,∗ , O.H. Gilja a,b a b
National Centre for Ultrasound in Gastroenterology, Department of Medicine, Haukeland University Hospital, 5021 Bergen, Norway Department of Clinical Medicine, University of Bergen, Bergen, Norway
a r t i c l e
i n f o
Article history: Received 12 April 2013 Accepted 14 May 2013 Keywords: Ultrasound Elastography Gastrointestinal tract
a b s t r a c t Ultrasound based elastography of the gastrointestinal tract may be a useful approach to improved tissue characterisation. Distinguishing malignant lesions from benign may be one useful application. Monitoring of inflammatory bowel lesions for degree of inflammation or fibrosis would be another clinically useful tool. The anatomy of the bowel, however, raises many challenges for strain or shear wave imaging due to thin structures, non-constant boundary conditions and intrinsic contractility. Pathological lesions tend to increase bowel wall thickness and may ease elastography imaging. Very few studies have addressed issues of bowel wall elastography so far, and both inflammatory and neoplastic lesions seem to increase tissue hardness in the bowel wall. © 2013 Elsevier Ireland Ltd. All rights reserved.
1. Introduction Ultrasonography of the wall of the GI tract shows a layered structure of 3–9 layers, depending on the frequency of the transducer used [1]. Usually 5 layers are observed representing from insideout, the interface between mucosa and lumen, the mucosa, the submucosa and two layers of muscularis propria [1]. When examining the intestines, it is sufficient to use frequencies of around 5 MHz, but preferably between 10 and 15 MHz, to enable optimal visualisation of wall layers, thickened bowel walls and target lesions. This also applies for strain imaging and, fortunately, the linear highfrequency external probes or endoluminal probes are usually well suited for elasticity imaging. 2. Methods of strain imaging Several methods for elasticity imaging have developed over the last years. Basically these methods can be divided into strain elastography [2] and shear-wave elastography [3,4]. Strain elastography methods map the shape change of the tissue over a time interval by tracking the echogenic spots in the B-mode image as the tissue is being exposed to a stretching or contracting force. When this is done manually the method is referred to as quasi-static elastography [2]. Induction of the contracting force may also be done by inflating a water filled balloon over the US transducer, such as in rectal scanning or by placing an acoustic pulse focused at the region of interest inside the organ [3]. In both cases, a strain or deformation map can be constructed and superimposed on the B-mode
∗ Corresponding author. Tel.: +47 559700. E-mail address: roald.fl[email protected] (R. Havre). 0720-048X/$ – see front matter © 2013 Elsevier Ireland Ltd. All rights reserved. http://dx.doi.org/10.1016/j.ejrad.2013.05.018
image. The other approach to strain imaging relies on approximations about the soft tissue as having a constant density and being incompressible like a fluid (Poisson constant, v = 0.5). Based on these assumptions, the Elastic modulus of the tissue may be calculated as proportional to the square of the shear wave speed [5]. Shear waves are qualitatively different from longitudinal waves, and they travel perpendicular to the direction of an ultrasonic pushpulse. The shear waves travel much slower than the longitudinal waves, and attenuate strongly over a short distance, which are factors that limit the lateral distribution of this image or measurement. On the other hand, shear wave imaging can provide qualitative elasticity data in terms of average shear wave speed or kilopascals in a limited area [6,7]. One producer of shear wave elastography provide a quantitative shear wave map by applying several “acoustic cones” of shear waves in the lateral direction providing a larger ROI with good lateral and axial elasticity data [4]. 3. Gastrointestinal wall pathology Because the bowel wall is a long and thin organ largely surrounded by the serosa on the outside and with a luminal inside frequently containing gas and food undergoing digestion, it is not an ideal organ to visualise with US elastography with the current methods. Both the serosa and the luminal side allow substantial movement, which may appear in elastography images as very soft tissue or even no-signal areas. One of the advantages of B-mode ultrasonography is the detailed visualisation of wall layers, but as the resolution of elastography generally is poorer than B-mode imaging, the same level of detail can usually not be obtained. Sometimes, a layered structure is observed in the elastography image but with poor correspondence to the B-mode layers. Because the bowel also has intrinsic peristaltic movements, a distinction between the
R. Havre, O.H. Gilja / European Journal of Radiology 83 (2014) 438–441
439
Fig. 1. Neuroendocrine carcinoma in the terminal ileum (T3). B-mode image (right) and elastogram (left). Examination was performed on resected tissue. Blue colour indicates harder tissue, red colour indicates softer tissue. Mean strain in tumour area A is compared to reference tissue B. The strain ratio (B/A) was 4.85. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of the article.)
stress induced movement and intrinsic movement may be difficult. However, the pathological bowel wall is more suitable for elastographic imaging. Pathological lesions usually induce a thickening of the bowel wall and reduced peristalsis, thus improving the conditions for strain imaging. 3.1. Tumour characterisation In the rectum tumours may represent adenomas or adenocarcinomas or a combination of the two. Trans-rectal ultrasound
represents a good imaging modality for T-staging and with the adjunct of elastography, it has shown ability to image cancerous tissue significantly harder than benign lesions [8]. This may be useful, especially in preoperative staging of small cancers and in the context of emerging treatment options such as trans-rectal endoscopic microsurgery. In the upper GI tract, the evaluation of intramural tumours by endoscopic ultrasonography (EUS) may become useful. If the tissue hardness can be shown to correspond with more aggressive gastrointestinal stromal tumours (GISTs) or better identification
Fig. 2. Intraoperative scan of an adenocarcinoma in the coecum. B-mode image (right) and elastogram (left). Tumour area is imaged with low strain indicating harder tissue than the surrounding reference tissue being pericolic fat and connective tissue. A strain ratio (B/A) of 5.14 was calculated between the reference tissue and tumour.
440
R. Havre, O.H. Gilja / European Journal of Radiology 83 (2014) 438–441
Fig. 3. External ultrasonography (right) and elastography (left) of a longitudinal section of a crohn stenosis in the terminal ileum. The thickened ileal-wall is hypoechoic on the B-mode image and shows low strain in the elastogram indicating harder tissue. The stenosis was removed surgically. Histology showed chronic ulcerating inflammation with granulomas, nodular lymphocyte aggregates and with increased amount of connective tissue in submucosa and subserosa. Strain ratio between peri-ileal fat (B) and bowel wall inflammatory stenosis (A) was 7.99.
of leiomyomas, lipomas, and aberrant pancreatic tissue, elastography may become useful in the upper GI tract. Currently, there are no reports on EUS of intramural lesions in the upper GI tract (Figs. 1 and 2). 3.2. Inflammation and fibrosis In inflammatory bowel disease (IBD) it has been proposed that elastography may enable better differentiation between fibrosis and active inflammation. Trans-abdominal elastography of the colon has also been reported with Real-Time Elastography, a strain elastography method was used in a rat animal model and could differentiate a chemically induced fibrosis (n = 6) different from chemically induced acute inflammation (n = 5). In humans with
Crohns disease, the method could differentiate between normal bowel and Crohn lesions [9]. However, the question of differentiation between predominantly fibrotic or inflammatory lesions was not addressed in this study. In another study using transcutaneous Real-Time Elastography on the colon wall in patients with Ulcerative Colitis, the authors reported correspondence between the elastography findings in terms of harder tissue signal and severity of inflammation by endoscopic scoring [10]. We conducted a study on surgically resected bowel lesions from patients with Crohn lesions (n = 9), adenocarcinomas (n = 16) and adenomas (n = 4). Both Crohn lesions and adenocarcinomas were harder than normal bowel wall and their immediate surrounding tissue. We could not distinguish between adenocarcinomas and Crohn lesions using strain-ratio for semi-quantification. Interestingly, a small
Fig. 4. Strain Rate Imaging analysis of relative strain in the gastric muscle layer by using a Doppler ultrasound method. A red dot in the inner layer of the proper muscle is drawn in the anterior part of the human antrum. In this contraction–relaxation cycle lasting approx. 9 s, a detailed mapping of strain increase and decrease was enabled showing a maximum 75% relative expansion of the tissue. One may appreciate that there is a difference in the time periods for the contraction (2/3) versus the relaxation phase (1/3).
R. Havre, O.H. Gilja / European Journal of Radiology 83 (2014) 438–441
number of adenomas were significantly softer than the adenocarcinomas in this ex vivo study [11]. Fig. 3 shows a trans-abdominal strain image of a Crohn lesion. The scientific basis of using strain imaging in order to diagnose predominance of inflammation differently from predominance of fibrosis in bowel wall lesions is yet very limited, and further studies are needed.
441
increase the bowel wall hardness. Weather ultrasound elastography may be used for differentiation between predominantly fibrotic or predominantly inflammatory lesions in IBD patients remains to be investigated. Conflicts of interest No conflicts of interests.
4. Gastrointestinal motility References The trans-abdominal application has been used for Strain rate imaging (SRI), which use tracking of tissue Doppler and preserving the sign of recorded strain in order to map contractions (negative strain) and relaxation/stretch (positive strain) [12]. Strain rate imaging is the temporal derivative of strain, i.e. it images the amount of strain per time unit. SRI is capable of differentiating between actively contracting muscle and passively following tissue. SRI enables separation of the contractile activity of the longitudinal and circular muscle layers, although this is not usually visible in B-mode. The SRI method was evaluated in vitro [13,14] and in vivo in response to drug intervention [12]. The method enabled visualisation and computation of of peristaltic activity and their relation to symptoms in patients with functional dyspepsia [15]. (Fig. 4) 5. Limitations of methods It is not possible to obtain a complete overview of all bowel segments using transabdominal ultrasound. Therefore, only selective segments of the intestines can be scanned. A major challenge to strain imaging of the bowel is peristaltic movements that introduce error in strain imaging. Also the thin structure of a normal bowel wall and the serosa and luminal surface that allows relatively large movements along these planes impairs at least strain based imaging. For endoscopic application, only strain elastography is available. Accordingly, more studies are needed to establish the role of strain imaging for the evaluation of GI pathology and motility. 6. Summary Imaging of the elastic properties in the GI tract may be technically demanding and not all of the current methods may be useful. Pathological lesions often represent areas of bowel wall thickening with reduced peristalsis, which enhance the applicability of elasticity imaging. Both neoplastic and inflammatory lesions may
[1] Odegaard S, Nesje LB, Lærum OD, Kimmey MB. High-frequency ultrasonographic imaging of the gastrointestinal wall. Expert Review of Medical Devices 2012;9(3):263–73. [2] Ophir J, Cespedes I, Ponnekanti H, Yazdi Y, Li X. Elastography: a quantitative method for imaging the elasticity of biological tissues. Ultrasonic Imaging 1991 Apr;13(2):111–34. [3] Palmeri ML, Frinkley KD, Zhai L, et al. Acoustic radiation force impulse (ARFI) imaging of the gastrointestinal tract. Ultrasonic Imaging 2005;27(April (2)):75–88. [4] Bercoff J, Tanter M, Fink M. Supersonic shear imaging: a new technique for soft tissue elasticity mapping. IEEE Transactions on Ultrasonics Ferroelectrics and Frequency Control 2004;51(April (4)):396–409. [5] Gennisson JL, Muller M, Deffieux T, Tanter M, Fink M. Quantitative viscoelasticity mapping of human liver using supersonic shear imaging: preliminary in vivo feasability study. Ultrasound in Medicine and Biology 2009;35(February (2)):219–29. [6] Gallotti A, D’Onofrio M, Pozzi Mucelli R. Acoustic radiation force impulse (ARFI) technique in ultrasound with Virtual Touch tissue quantification of the upper abdomen. La Radiologia Medica 2010;115(September (6)):889–97. [7] Palmeri ML, Nightingale KR. Acoustic radiation force-based elasticity imaging methods. Interface Focus 2011;1(August (4)):553–64. [8] Waage JE, Havre RF, Odegaard S, Leh S, Eide GE, Baatrup G. Endorectal elastography in the evaluation of rectal tumours. Colorectal Disease 2011;13(Octtober (10)):1130–7. [9] Stidham RW, Xu J, Johnson LA, et al. Ultrasound elasticity imaging for detecting intestinal fibrosis and inflammation in rats and humans with Crohn’s disease. Gastroenterology 2011;141(September (3)):819–26, e1. [10] Rustemovic N, Cukovic-Cavka S, Brinar M, et al. A pilot study of transrectal endoscopic ultrasound elastography in inflammatory bowel disease. BMC Gastroenterol 2011;11(October (1)):113. [11] Havre RF, Leh S, Gilja OH, et al. Strain assessment in surgically resected inflammatory and neoplastic bowel lesions. Ultraschall in der Medizin 2011. Epub Nov 15. [12] Ahmed AB, Gilja OH, Hausken T, Gregersen H, Matre K. Strain measurement during antral contractions by ultrasound strain rate imaging: influence of erythromycin. Neurogastroenterology & Motility 2009;21(February (2)):170–9. [13] Matre K, Ahmed AB, Gregersen H, et al. In vitro evaluation of ultrasound Doppler strain rate imaging: modification for measurement in a slowly moving tissue phantom. Ultrasound in Medicine and Biology 2003;29(December (12)):1725–34. [14] Ahmed AB, Gilja OH, Gregersen H, Odegaard S, Matre K. In vitro strain measurement in the porcine antrum using ultrasound doppler strain rate imaging. Ultrasound in Medicine and Biology 2006;32(April (4)):513–22. [15] Gilja OH. Ultrasound of the stomach – The EUROSON lecture 2006. Ultraschall in der Medizin 2007;28(February (1)):32–9.
Contents lists available at ScienceDirect
European Journal of Radiology journal homepage: www.elsevier.com/locate/ejrad
Elastography and strain rate imaging of the gastrointestinal tract R. Havre a,∗ , O.H. Gilja a,b a b
National Centre for Ultrasound in Gastroenterology, Department of Medicine, Haukeland University Hospital, 5021 Bergen, Norway Department of Clinical Medicine, University of Bergen, Bergen, Norway
a r t i c l e
i n f o
Article history: Received 12 April 2013 Accepted 14 May 2013 Keywords: Ultrasound Elastography Gastrointestinal tract
a b s t r a c t Ultrasound based elastography of the gastrointestinal tract may be a useful approach to improved tissue characterisation. Distinguishing malignant lesions from benign may be one useful application. Monitoring of inflammatory bowel lesions for degree of inflammation or fibrosis would be another clinically useful tool. The anatomy of the bowel, however, raises many challenges for strain or shear wave imaging due to thin structures, non-constant boundary conditions and intrinsic contractility. Pathological lesions tend to increase bowel wall thickness and may ease elastography imaging. Very few studies have addressed issues of bowel wall elastography so far, and both inflammatory and neoplastic lesions seem to increase tissue hardness in the bowel wall. © 2013 Elsevier Ireland Ltd. All rights reserved.
1. Introduction Ultrasonography of the wall of the GI tract shows a layered structure of 3–9 layers, depending on the frequency of the transducer used [1]. Usually 5 layers are observed representing from insideout, the interface between mucosa and lumen, the mucosa, the submucosa and two layers of muscularis propria [1]. When examining the intestines, it is sufficient to use frequencies of around 5 MHz, but preferably between 10 and 15 MHz, to enable optimal visualisation of wall layers, thickened bowel walls and target lesions. This also applies for strain imaging and, fortunately, the linear highfrequency external probes or endoluminal probes are usually well suited for elasticity imaging. 2. Methods of strain imaging Several methods for elasticity imaging have developed over the last years. Basically these methods can be divided into strain elastography [2] and shear-wave elastography [3,4]. Strain elastography methods map the shape change of the tissue over a time interval by tracking the echogenic spots in the B-mode image as the tissue is being exposed to a stretching or contracting force. When this is done manually the method is referred to as quasi-static elastography [2]. Induction of the contracting force may also be done by inflating a water filled balloon over the US transducer, such as in rectal scanning or by placing an acoustic pulse focused at the region of interest inside the organ [3]. In both cases, a strain or deformation map can be constructed and superimposed on the B-mode
∗ Corresponding author. Tel.: +47 559700. E-mail address: roald.fl[email protected] (R. Havre). 0720-048X/$ – see front matter © 2013 Elsevier Ireland Ltd. All rights reserved. http://dx.doi.org/10.1016/j.ejrad.2013.05.018
image. The other approach to strain imaging relies on approximations about the soft tissue as having a constant density and being incompressible like a fluid (Poisson constant, v = 0.5). Based on these assumptions, the Elastic modulus of the tissue may be calculated as proportional to the square of the shear wave speed [5]. Shear waves are qualitatively different from longitudinal waves, and they travel perpendicular to the direction of an ultrasonic pushpulse. The shear waves travel much slower than the longitudinal waves, and attenuate strongly over a short distance, which are factors that limit the lateral distribution of this image or measurement. On the other hand, shear wave imaging can provide qualitative elasticity data in terms of average shear wave speed or kilopascals in a limited area [6,7]. One producer of shear wave elastography provide a quantitative shear wave map by applying several “acoustic cones” of shear waves in the lateral direction providing a larger ROI with good lateral and axial elasticity data [4]. 3. Gastrointestinal wall pathology Because the bowel wall is a long and thin organ largely surrounded by the serosa on the outside and with a luminal inside frequently containing gas and food undergoing digestion, it is not an ideal organ to visualise with US elastography with the current methods. Both the serosa and the luminal side allow substantial movement, which may appear in elastography images as very soft tissue or even no-signal areas. One of the advantages of B-mode ultrasonography is the detailed visualisation of wall layers, but as the resolution of elastography generally is poorer than B-mode imaging, the same level of detail can usually not be obtained. Sometimes, a layered structure is observed in the elastography image but with poor correspondence to the B-mode layers. Because the bowel also has intrinsic peristaltic movements, a distinction between the
R. Havre, O.H. Gilja / European Journal of Radiology 83 (2014) 438–441
439
Fig. 1. Neuroendocrine carcinoma in the terminal ileum (T3). B-mode image (right) and elastogram (left). Examination was performed on resected tissue. Blue colour indicates harder tissue, red colour indicates softer tissue. Mean strain in tumour area A is compared to reference tissue B. The strain ratio (B/A) was 4.85. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of the article.)
stress induced movement and intrinsic movement may be difficult. However, the pathological bowel wall is more suitable for elastographic imaging. Pathological lesions usually induce a thickening of the bowel wall and reduced peristalsis, thus improving the conditions for strain imaging. 3.1. Tumour characterisation In the rectum tumours may represent adenomas or adenocarcinomas or a combination of the two. Trans-rectal ultrasound
represents a good imaging modality for T-staging and with the adjunct of elastography, it has shown ability to image cancerous tissue significantly harder than benign lesions [8]. This may be useful, especially in preoperative staging of small cancers and in the context of emerging treatment options such as trans-rectal endoscopic microsurgery. In the upper GI tract, the evaluation of intramural tumours by endoscopic ultrasonography (EUS) may become useful. If the tissue hardness can be shown to correspond with more aggressive gastrointestinal stromal tumours (GISTs) or better identification
Fig. 2. Intraoperative scan of an adenocarcinoma in the coecum. B-mode image (right) and elastogram (left). Tumour area is imaged with low strain indicating harder tissue than the surrounding reference tissue being pericolic fat and connective tissue. A strain ratio (B/A) of 5.14 was calculated between the reference tissue and tumour.
440
R. Havre, O.H. Gilja / European Journal of Radiology 83 (2014) 438–441
Fig. 3. External ultrasonography (right) and elastography (left) of a longitudinal section of a crohn stenosis in the terminal ileum. The thickened ileal-wall is hypoechoic on the B-mode image and shows low strain in the elastogram indicating harder tissue. The stenosis was removed surgically. Histology showed chronic ulcerating inflammation with granulomas, nodular lymphocyte aggregates and with increased amount of connective tissue in submucosa and subserosa. Strain ratio between peri-ileal fat (B) and bowel wall inflammatory stenosis (A) was 7.99.
of leiomyomas, lipomas, and aberrant pancreatic tissue, elastography may become useful in the upper GI tract. Currently, there are no reports on EUS of intramural lesions in the upper GI tract (Figs. 1 and 2). 3.2. Inflammation and fibrosis In inflammatory bowel disease (IBD) it has been proposed that elastography may enable better differentiation between fibrosis and active inflammation. Trans-abdominal elastography of the colon has also been reported with Real-Time Elastography, a strain elastography method was used in a rat animal model and could differentiate a chemically induced fibrosis (n = 6) different from chemically induced acute inflammation (n = 5). In humans with
Crohns disease, the method could differentiate between normal bowel and Crohn lesions [9]. However, the question of differentiation between predominantly fibrotic or inflammatory lesions was not addressed in this study. In another study using transcutaneous Real-Time Elastography on the colon wall in patients with Ulcerative Colitis, the authors reported correspondence between the elastography findings in terms of harder tissue signal and severity of inflammation by endoscopic scoring [10]. We conducted a study on surgically resected bowel lesions from patients with Crohn lesions (n = 9), adenocarcinomas (n = 16) and adenomas (n = 4). Both Crohn lesions and adenocarcinomas were harder than normal bowel wall and their immediate surrounding tissue. We could not distinguish between adenocarcinomas and Crohn lesions using strain-ratio for semi-quantification. Interestingly, a small
Fig. 4. Strain Rate Imaging analysis of relative strain in the gastric muscle layer by using a Doppler ultrasound method. A red dot in the inner layer of the proper muscle is drawn in the anterior part of the human antrum. In this contraction–relaxation cycle lasting approx. 9 s, a detailed mapping of strain increase and decrease was enabled showing a maximum 75% relative expansion of the tissue. One may appreciate that there is a difference in the time periods for the contraction (2/3) versus the relaxation phase (1/3).
R. Havre, O.H. Gilja / European Journal of Radiology 83 (2014) 438–441
number of adenomas were significantly softer than the adenocarcinomas in this ex vivo study [11]. Fig. 3 shows a trans-abdominal strain image of a Crohn lesion. The scientific basis of using strain imaging in order to diagnose predominance of inflammation differently from predominance of fibrosis in bowel wall lesions is yet very limited, and further studies are needed.
441
increase the bowel wall hardness. Weather ultrasound elastography may be used for differentiation between predominantly fibrotic or predominantly inflammatory lesions in IBD patients remains to be investigated. Conflicts of interest No conflicts of interests.
4. Gastrointestinal motility References The trans-abdominal application has been used for Strain rate imaging (SRI), which use tracking of tissue Doppler and preserving the sign of recorded strain in order to map contractions (negative strain) and relaxation/stretch (positive strain) [12]. Strain rate imaging is the temporal derivative of strain, i.e. it images the amount of strain per time unit. SRI is capable of differentiating between actively contracting muscle and passively following tissue. SRI enables separation of the contractile activity of the longitudinal and circular muscle layers, although this is not usually visible in B-mode. The SRI method was evaluated in vitro [13,14] and in vivo in response to drug intervention [12]. The method enabled visualisation and computation of of peristaltic activity and their relation to symptoms in patients with functional dyspepsia [15]. (Fig. 4) 5. Limitations of methods It is not possible to obtain a complete overview of all bowel segments using transabdominal ultrasound. Therefore, only selective segments of the intestines can be scanned. A major challenge to strain imaging of the bowel is peristaltic movements that introduce error in strain imaging. Also the thin structure of a normal bowel wall and the serosa and luminal surface that allows relatively large movements along these planes impairs at least strain based imaging. For endoscopic application, only strain elastography is available. Accordingly, more studies are needed to establish the role of strain imaging for the evaluation of GI pathology and motility. 6. Summary Imaging of the elastic properties in the GI tract may be technically demanding and not all of the current methods may be useful. Pathological lesions often represent areas of bowel wall thickening with reduced peristalsis, which enhance the applicability of elasticity imaging. Both neoplastic and inflammatory lesions may
[1] Odegaard S, Nesje LB, Lærum OD, Kimmey MB. High-frequency ultrasonographic imaging of the gastrointestinal wall. Expert Review of Medical Devices 2012;9(3):263–73. [2] Ophir J, Cespedes I, Ponnekanti H, Yazdi Y, Li X. Elastography: a quantitative method for imaging the elasticity of biological tissues. Ultrasonic Imaging 1991 Apr;13(2):111–34. [3] Palmeri ML, Frinkley KD, Zhai L, et al. Acoustic radiation force impulse (ARFI) imaging of the gastrointestinal tract. Ultrasonic Imaging 2005;27(April (2)):75–88. [4] Bercoff J, Tanter M, Fink M. Supersonic shear imaging: a new technique for soft tissue elasticity mapping. IEEE Transactions on Ultrasonics Ferroelectrics and Frequency Control 2004;51(April (4)):396–409. [5] Gennisson JL, Muller M, Deffieux T, Tanter M, Fink M. Quantitative viscoelasticity mapping of human liver using supersonic shear imaging: preliminary in vivo feasability study. Ultrasound in Medicine and Biology 2009;35(February (2)):219–29. [6] Gallotti A, D’Onofrio M, Pozzi Mucelli R. Acoustic radiation force impulse (ARFI) technique in ultrasound with Virtual Touch tissue quantification of the upper abdomen. La Radiologia Medica 2010;115(September (6)):889–97. [7] Palmeri ML, Nightingale KR. Acoustic radiation force-based elasticity imaging methods. Interface Focus 2011;1(August (4)):553–64. [8] Waage JE, Havre RF, Odegaard S, Leh S, Eide GE, Baatrup G. Endorectal elastography in the evaluation of rectal tumours. Colorectal Disease 2011;13(Octtober (10)):1130–7. [9] Stidham RW, Xu J, Johnson LA, et al. Ultrasound elasticity imaging for detecting intestinal fibrosis and inflammation in rats and humans with Crohn’s disease. Gastroenterology 2011;141(September (3)):819–26, e1. [10] Rustemovic N, Cukovic-Cavka S, Brinar M, et al. A pilot study of transrectal endoscopic ultrasound elastography in inflammatory bowel disease. BMC Gastroenterol 2011;11(October (1)):113. [11] Havre RF, Leh S, Gilja OH, et al. Strain assessment in surgically resected inflammatory and neoplastic bowel lesions. Ultraschall in der Medizin 2011. Epub Nov 15. [12] Ahmed AB, Gilja OH, Hausken T, Gregersen H, Matre K. Strain measurement during antral contractions by ultrasound strain rate imaging: influence of erythromycin. Neurogastroenterology & Motility 2009;21(February (2)):170–9. [13] Matre K, Ahmed AB, Gregersen H, et al. In vitro evaluation of ultrasound Doppler strain rate imaging: modification for measurement in a slowly moving tissue phantom. Ultrasound in Medicine and Biology 2003;29(December (12)):1725–34. [14] Ahmed AB, Gilja OH, Gregersen H, Odegaard S, Matre K. In vitro strain measurement in the porcine antrum using ultrasound doppler strain rate imaging. Ultrasound in Medicine and Biology 2006;32(April (4)):513–22. [15] Gilja OH. Ultrasound of the stomach – The EUROSON lecture 2006. Ultraschall in der Medizin 2007;28(February (1)):32–9.