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Acoustic Radiation Force Impulse (ARFI) Imaging of the Gastrointestinal Tract Mark Palmeri, Kristin Frinkley, Liang Zhai, Rex Bentley, Kirk Ludwig, Marcia Gottfried, and Kathryn Nightingale Duke University, Durham, NC 27708 firstname.lastname@example.org Abstract— Currently, the evaluation of lesions in the gastroin- trointestinal (GI) tract are most commonly imaged using testinal (GI) tract using ultrasound suffers from poor contrast endoscopic ultrasound (EUS) , ; however, EUS can suffer between healthy and diseased tissue. Acoustic Radiation Force from poor contrast between healthy and diseased tissues in Impulse (ARFI) imaging provides information about the me- chanical properties of tissue using brief, high-intensity, focused the GI tract. The organs of the GI tract are layered; from ultrasound to generate radiation force, and conventional, ultra- the lumen outward, these layers consist of the mucosa (1-2 sonic, correlation-based methods to track tissue displacement. mm thick), submucosa (∼2 mm thick), muscularis propria (2- Using conventional linear arrays, ARFI imaging has shown 3 mm thick), and the adventitia. GI cancers are staged by improved contrast over B-mode images when applied to solid degree of tumor invasion (T-staging) into the layers of the masses in the breast and liver. The purpose of this work is to (1) demonstrate that ARFI imaging can be performed with bowel wall, along with determining the potential spread of an endocavity probe, and (2) demonstrate that ARFI imaging malignant cells to local lymph nodes (N-staging). The most can provide improvements over conventional B-mode imaging of critical staging distinction must be made between stage uT2 GI lesions. An EC94, 6.2 MHz, endocavity probe was modiﬁed and uT3 tumors, which indicates whether or not a tumor has to perform ARFI imaging in tissue-mimicking phantoms using penetrated through the muscularis propria. For rectal cancers, a Siemens SONOLINE AntaresTM scanner. ARFI imaging was this distinction determines whether a patient will undergo local performed on fresh, surgically-excised, GI lesions using a 75L40, 7.2 MHz, linear array on a modiﬁed Siemens SONOLINE tumor excision, or neoadjuvant chemotherapy and radiation, ElegraTM scanner. The endocavity probe created ARFI images followed by radical resection . The latter treatment option to a depth of over 2 cm in tissue-mimicking phantoms, with is associated with greater risks to the patient, including infec- maximum displacements of 5 µm. The endocavity probe did not tion, bleeding, decreased colonic motility, and incontinence. heat appreciably during ARFI imaging, demonstrating that the Treating a stage uT2 tumor as a uT3 tumor unnecessarily probe’s small size will not limit in vivo ARFI imaging. ARFI im- ages of an adenocarcinoma of the gastroesophageal (GE) junction, subjects a patient to these risks; however, staging uT2 cancers status-post chemotherapy and radiation treatment, demonstrate as uT3 occurs in 10-35% of EUS scans , , leading better contrast between healthy and ﬁbrotic/malignant tissue to overly-aggressive medical treatments and surgeries. The than standard B-mode images. ARFI images of healthy gastric, National Cancer Institute has established a research priority to esophageal, and colonic tissue specimens differentiate normal improve the staging of colorectal tumors to more accurately anatomic tissue planes (i.e., mucosal, muscularis, and adventitial layers), as conﬁrmed by histologic evaluation. ARFI imaging of an guide treatment decisions . Applying ARFI imaging to the ex vivo colon cancer portrays interesting contrast and structure GI tract may provide such an improvement by more clearly not present in B-mode images. These ﬁndings support the clinical delineating healthy tissue layers and the penetration of tumors feasibility of endoscopic ARFI imaging to guide diagnosis and into those tissue layers. staging of disease processes in the GI tract. II. M ETHODS I. I NTRODUCTION & BACKGROUND A. Experimental Acoustic Radiation Force Impulse (ARFI) imaging is one of ARFI imaging of freshly-excised, surgical specimens was many acoustic radiation force-based imaging modalities being performed using a Siemens 75L40 linear array (7.2 MHz, studied to generate images of the mechanical properties of F/1.3 focal conﬁguration) on a Siemens SONOLINE ElegraTM tissue . ARFI imaging uses short-duration (< 100 µs), high- Scanner (Siemens Medical Solutions USA, Inc., Ultrasound intensity, acoustic pulses to generate localized, micron-scale Division, Issaquah, WA). The system was modiﬁed to control displacements in tissue, and these displacements are tracked acoustic beam sequences and intensities, and raw Radio Fre- using ultrasonic, correlation-based methods . Images of quency (RF) data was stored and processed off-line. Data was two-dimensional regions of interest are generated by sequen- acquired sequentially, as is done in conventional ultrasound tially interrogating multiple lateral locations, as is done in imaging. At each lateral location, a reference tracking beam color Doppler imaging. was ﬁred, followed by a high-intensity pushing beam that Potentially malignant lesions and lymph nodes of the gas- displaced the tissue. A series of tracking beams followed the pushing beam to track the tissue recovery for 4 ms with a Mucosa −> Pulse Repetition Frequency (PRF) of 5632 Hz. Submucosa −> The transducer was held in a ﬁxed ring-stand, while the sur- MP gical specimens were placed on top of a water bag. Ultrasonic gel was used to couple the transducer to the specimens. When Fibrosis Muscularis Propria (MP) possible, surgical specimens were marked with dissection ink so that histologic sections could be made in the imaging plane. Adventitia ARFI imaging was also performed using a Siemens EC94 endocavity probe (6.2 MHz, F/1.5 focal conﬁguration, 30 mm elevation focus) on a Siemens SONOLINE AntaresTM 5 Depth (mm) Scanner. Imaging was performed on a gelatin-based, tissue- 10 mimicking phantom containing a stiffer, spherical inclusion. 15 The fabrication of such phantoms is outlined by Hall et al. . 20 0 10 20 30 40 50 60 70 Lateral Position (mm) B. Finite Element Modeling 20 Finite element models were developed to evaluate ARFI 5 MP Depth (mm) MP imaging performance for different transducers, system param- 10 10 A eters, and tissue mechanical and acoustic properties . Field 15 II (http://www.es.oersted.dtu.dk/staff/jaj/ﬁeld/)  was used 20 0 0 10 20 30 40 50 60 70 to solve for the three-dimensional, high-intensity, focused, Lateral Position (mm) acoustic ﬁelds generated during ARFI imaging. A rectilinear 1.2 mesh with uniform 0.2 mm node spacing was generated using 5 1 Depth (mm) LS-PREPOST (Livermore Software Technology Corporation, 10 0.8 0.6 Livermore, CA). The mesh material properties were deﬁned 15 0.4 0.2 to simulate a three-layer, elastic structure, as speciﬁed in 20 0 10 20 30 40 50 60 70 Table I, with the Young’s moduli being rough estimates of Lateral Position (mm) the stiffnesses of mucosal, muscularis, and adventitial layers. No slippage was allowed between the material layers in this 5 1.5 Depth (mm) preliminary model. 10 1 15 0.5 TABLE I 20 0 10 20 30 40 50 60 70 F INITE E LEMENT M ODEL M ATERIAL P ROPERTIES Lateral Position (mm) Depth from Young’s Modulus Poisson’s Ratio Lumen (mm) (kPa) Fig. 1. From top to bottom: Photo of gross tissue specimen (top left); H&E 0-1 1.0 0.499 stain of esophageal side of the ulceration dissected in the imaging plane, 1-5 16.0 0.499 as indicated by the break in the dashed line in the gross photo (top right); 5 - 25 4.0 0.499 Matched B-mode image; ARFI maximum displacement image (µm); ARFI time-to-peak displacement image (ms); and ARFI recovery time image (ms) of an ex vivo, status-post chemotherapy and radiation, adenocarcinoma in the gastroesophageal junction. The histology image demonstrates disruption of the III. R ESULTS & D ISCUSSION mucosal, submucosal and muscular layers by stiffer, ﬁbrotic scar tissue. Note the boundary deﬁnition in the three visualized layers of the stomach (left) in Fig. 1 shows an ex vivo gastroesophageal (GE) junction the ARFI displacement image. Note also the thin black line separating the with an ulcerated adenocarcinoma, status-post chemotherapy peri-adventitial tissue from the bottom layer of the muscularis propria. The top gel bridge and bottom gauze have been masked in black. and radiation treatment. ARFI images were created down the dashed, black line in the upper-left image (Fig. 1), with the stomach on the left-hand side of the ARFI images, and the esophagus on the right-hand side of the images. Histologic improved delineation of the tissue layers in the ARFI image. correlation was provided in the imaging plane along the break The bottom row shows an enlarged region of the upper right in the dashed line. Notice that in the healthy stomach, the ARFI displacement image (left), and the normalized axial anatomical layers of the gastric tissue can be delineated (left displacements averaged across the region indicated by the side, gray layers). These layers become interrupted in the vertical dashed lines (right). The regions of decreased displace- ulcerated region by stiffer, ﬁbrotic tissue, which then gives ment in the submucosal layer (15 - 17 mm) may correspond way to healthy, esophageal tissue on the right. These layers to stiffer lymphoid aggregates. Better layer distinction with can be visualized in the ARFI images, as conﬁrmed by the ARFI imaging may allow for more accurate staging of tumor histology image. invasion. The top row of Fig. 2 shows a comparison of B-mode Fig. 3 shows B-mode and ARFI images for an ex vivo cecal and ARFI images for normal, proximal colon tissue, with colon with a uT3/N- tumor, for three different locations in the B−mode ARFI Displacement (0.7 ms) Fig. 4 shows matched B-mode and ARFI displacement Depth (mm) 15 15 images of a breast lymph node. Note the detailed structure 20 20 of the hilum and efferent duct present in the ARFI image (white arrow). The ability to image structural and material −10 0 10 −10 0 10 Lateral Position (mm) Lateral Position (mm) properties of lymph nodes may allow ARFI imaging to help ARFI Displacement (t=0.7 ms) with N-staging of lymph nodes. 14 14 Max Disp B−mode (~5 µm) 15 15 4 4 6 6 16 16 8 8 Depth (mm) 17 17 10 10 depth, (mm) Depth (mm) 12 12 18 18 14 14 16 16 19 19 18 18 20 20 20 20 22 22 21 21 −10 −5 0 5 10 −10 −5 0 5 10 lateral position, (mm) 22 22 Lateral Position (mm) −5 0 5 0 50 100 Lateral Position (mm) ARFI Displacement (µm) Fig. 4. B-mode (left) and matched ARFI maximum displacement image Fig. 2. The top row shows matched B-mode (left) and ARFI displacement (right) of an in vivo, biopsy-proven reactive lymph node in the breast. The (right) images of a normal section of proximal colon. The ARFI image was lymph node is the darker oval region in the B-mode image appearing from 12- 0.7 ms after excitation. The lower left image shows an enlarged region of 22 mm in depth, with a central, more echoic region. The echogenic center in the upper right ARFI displacement image. The lower right image shows a the B-mode image is a sign of normal hilar structure. The hilum corresponds normalized axial displacement proﬁle, averaged across the region indicated to a region of decreased displacement in the ARFI image (darker region). The by the vertical dashed lines. Notice the greater structural contrast between node itself appears slightly stiffer (darker) than the surrounding tissue, with layers in the ARFI images compared with the B-mode image. The mucosa a ductal, stiff structure (arrow) extending from the dark core to the edge of spans from 14 - 15 mm, the submucosa from 15 - 17 mm, and the muscularis the node. propria from 17 - 19 mm, followed by deeper adventitial tissue. Also notice regions of increased stiffness in the submucosal layer that may correspond to Fig. 5 shows ARFI images generated with the Siemens stiffer lymphoid aggregates. EC94 endocavity probe in a gelatin-based, tissue-mimicking phantom. These images demonstrate that smaller, endocavity arrays can deliver enough energy to generate ARFI images. tumor. Notice that the ARFI images show much better contrast There was not appreciable heating of the endocavity probe between structures than the B-mode images. during these experiments, further supporting the feasibility of in vivo ARFI imaging. B−mode ARFI Disp (t=0.7ms,~5µm) 5 5 Displacement Recovery 10 10 B−mode (~5 µm, t=0.7ms) (t = 1.3 ms) 15 15 Axial Depth (mm) 15 20 20 −10 0 10 −10 0 10 5 5 Depth (mm) 20 10 10 15 15 25 20 20 −10 0 10 −10 0 10 5 5 −5 0 5 −5 0 5 −5 0 5 Lateral Position (mm) 10 10 15 15 Fig. 5. Matched B-mode and ARFI images of a gelatin-based, tissue- mimicking phantom with a 5 mm spherical inclusion that is approximately 20 20 three times stiffer than the background material. These images were generated −10 0 10 −10 0 10 Lateral Position (mm) Lateral Position (mm) using the Antares scanner and an EC94, 6.2 MHz, end-looking, endocavity transducer. Fig. 3. B-mode (left) and ARFI (right) images of an excised uT3/N- colon tumor near the cecal pouch. The top row of images show stiff tumor tissue Fig. 6 shows simulated displacement proﬁles along the surrounded by softer tumor tissue that extends down to a very soft layer axial-lateral plane, centered in elevation in homogeneous (E = of presumed adventitial fat. These images were acquired over a region of palpably stiff and tethered tumor. Notice the surrounding tumor has replaced 4.0 kPa, left) and layered materials (Table I, right). In contrast normal tissue layers of the colon, shown in Fig. 2. The middle images show to 2-D ARFI images, these images show the 2-D displace- tumor that disrupts a normal dark band of tissue (possibly the distal boundary ment ﬁeld generated by a single ARFI push with subsequent of the muscularis propria) at a depth of ∼14 mm. Again, the normal layers of the colon have been replaced by tumor tissue. The bottom images demonstrate shear wave propagation at later times. Notice the decreased structural features in the ARFI image not present in the B-mode image in displacement conﬁned to the stiffer, middle layer (right), regions where tumor and healthy tissue may be interspersed. indicating that ARFI imaging could provide information about the location of layers with different material properties. Also R EFERENCES notice that through time, shear waves propagate away from the  D. Blumberg and R. Ramanathan. Treatment of colon and rectal cancer. region of excitation (ROE) with a faster velocity in the stiffer J Clin Gastroenterol, 34(1):15–26, 2002. (middle layer) material than the softer surrounding material.  J. Garcia-Aguilar, J. Pollack, S. Lee, E. Hernandez de Anda, A. Mell- gren, W. Wong, C. Finne, D. Rothenberger, and R. Madoff. Accuracy This highlights another metric that ARFI imaging may use to of endorectal ultrasonography in preoperative staging of rectal tumors. generate images delineating the tissue layers of the GI tract. Dis. Colon Rectum, 45(1):10–15, 2002.  P. Gibbs, M. Chao, and J. Tjandra. Optimizing the outcome for patients with rectal cancer. Dis. Colon Rectum, 46(3):389–402, 2003.  Hall T.J., Bilgen M., Insana M.F., and Krouskop T.A. Phantom materials 5 5 for elastography. IEEE Transactions on Ultrasonics, Ferroelectrics and 10 10 Frequency Control, 44(6):1355–65, 1997.  F. Hulsmans, T. Tio, P. Fockens, A. Bosma, and G. Tytgat. Assessment 15 15 of tumor inﬁltration depth in rectal cancer with transrectal sonography: Caution is necessary. Radiology, 190(3):715:720, 1994. Depth (mm)  N. C. Institute, O. of Science Planning, and Assess- 5 5 ment. Colorectal cancer, progress review groups, 2004. http://prg.nci.nih.gov/colorectal/default.html. 10 10  J. Jensen and N. Svendsen. Calculation of pressure ﬁelds from arbitrarily 15 15 shaped, apodized, and excited ultrasound transducers. IEEE Trans. Ultrason., Ferroelec., Freq. Contr., 39(2):262–267, 1992.  D. Malfair, A. Jacqueline, and P. Phang. Preoperative rectal cancer 5 5 imaging. BC Medical Journal, 45(6):259–261, 2003.  K. Nightingale, M. Palmeri, R. Nightingale, and G. Trahey. On the 10 10 feasibility of remote palpation using acoustic radiation force. J. Acoust. 15 15 Soc. Am., 110(1):625–634, 2001. −5 0 5 −5 0 5  K. Nightingale, M. Soo, R. Nightingale, and G. Trahey. Acoustic Lateral Position (mm) Lateral Position (mm) radiation force impulse imaging: In vivo demonstration of clinical feasibility. Ultrasound Med. Biol., 28(2):227–235, 2002. Fig. 6. Simulated, normalized axial displacement ﬁelds generated from  M. Palmeri and K. Nightingale. A ﬁnite element method model of a single ARFI excitation on the axial-lateral plane, centered in elevation, soft tissue response to impulsive acoustic radiation force. IEEE Trans. comparing a homogeneous medium (4 kPa, left side) and the layered model Ultrason., Ferroelec., Freq. Contr., in review. (right side, layer interfaces indicated by the dashed lines). The rows indicate displacements at 5 ms, 10 ms, and 15 ms post-excitation in the top, middle, and bottom rows, respectively. Notice the decreased displacement within the middle layer, in the right-hand column, as compared with the softer, homogeneous model (left column). Also notice the faster shear wave velocity in the stiffer, middle layer as compared with the softer surrounding layers. IV. C ONCLUSION ARFI imaging can be used to delineate the normal tissue layers of the GI tract in esophageal, gastric, and colonic tissues. ARFI images correlate well with histology in imaging spatial extent of stiff, ﬁbrotic scar tissue in the GE junction. Furthermore, ARFI images show the boundaries of colonic tumors, providing a potential mechanical metric to improve ultrasonic tumor staging (T-staging). Compared with B-mode imaging, ARFI imaging more clearly illustrates internal struc- tural information in lymph nodes, with the clinical motivation of improving N-staging. ARFI imaging has been implemented on an endocavity probe. Finally, FEM models demonstrate that ARFI imaging is capable of distinguishing layers of varying material properties through both displacement maps and shear wave velocities. Overall, ARFI imaging appears promising for improving the staging of GI tumors and lymph nodes. V. ACKNOWLEDGMENTS This work was supported by NIH grant 8 R01 EB002132, the Whitaker Foundation, and the Medical Scientist Training Program grant T 32 GM-07171. We thank Dr. Gregg Trahey for his valuable insight, and Siemens Medical Solutions USA, Inc., Ultrasound Division for their technical assistance.
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