- Email: [email protected]
GI magnetic resonance angiography
GI magnetic resonance angiography Charles M. Anderson, MD, PhD San Francisco, California
MRA is a type of magnetic resonance imaging (MRI) in which blood appears bright. To form a magnetic resonance (MR) angiogram, a 3-dimensional set of thin sections is acquired through the region of interest. The images are then processed by computer to create a 2-dimensional projected display that resembles a conventional angiogram. There are many ways to cause blood to appear bright on MRI. Each of these mechanisms corresponds to a different type of MRA. Brightness may result from the entry of blood into the section. This mechanism is responsible for the time-of-flight (TOF) methods.1 Brightness may be dependent on the velocity of blood, which is the principle behind phase-contrast (PC) MRA.2 Brightness may result from the injection of contrast agents, which is the basis for contrast-enhanced MRA (CEMRA).3 Other mechanisms exist as well, although they are much less common than these three. In recent years, CEMRA has emerged as the dominant MRA method. CEMRA is applicable to nearly every abdominal vessel, including the aorta, renal arteries, mesenteric arteries, and portal vein.4 CEMRA is much faster than TOF and PC. It is accomplished in a single breath hold and so is less exhausting to the patient, as compared with TOF, which may require a separate breath hold for each section. CEMRA is demonstrably better than TOF or PC in the imaging of arterial branch vessels. Furthermore, it resembles conventional angiography and CT angiography (CTA), both of which use the same principle of blood enhancement by intravascular contrast agents. NONINVASIVE VASCULAR IMAGING Vascular imaging of the abdomen was once the exclusive domain of catheter angiography, but is now performed more safely and cheaply by noninvasive Doppler ultrasound (DUS), MRA, or CTA. Each of these noninvasive modalities has its own strengths and favored applications. From the San Francisco VA Medical Center, San Francisco, California. Reprint requests to: Charles M. Anderson, MD, PhD, Radiology (114), SFVAMC, 4150 Clement St, San Francisco, CA 94121. 37/0/124744 doi:10.1067/mge.2002.124744 S42
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DUS is the first choice for liver vessel imaging, particularly when measurement of velocity and direction of flow is required. Velocities are used to evaluate of portal hypertension and to assess the function of transjugular intrahepatic portosystemic shunts (TIPS). Ultrasound plays a limited role in splanchnic vessel imaging as a result of overlying bowel gas, which impedes the acoustic signal.5 MRA and CTA provide rapid 3-dimensional angiograms of the aorta and its proximal mesenteric branches, as well as of the portosplenic veins and varices. In most cases, MRA and CTA provide equivalent vascular information. The choice of using MRA or CTA is usually based on imaging considerations other than vascular. For example: Unlike CTA, MRA does not use iodinated contrast, and so is indicated for patients with renal insufficiency or who have an allergy to iodinated contrast preparations. Iodinated contrast is also undesirable in the event that an interventional procedure must be performed on the same day, for example to embolize a bleeding artery, because the intervention will also require the injection of iodinated contrast material. CTA allows open access to the critically ill patient who may require close physiological monitoring. In MRA, physical access to the patient within the bore of the magnet is limited. In addition, the critically ill patient may not be able to hold his or her breath for the approximately 15 seconds required to perform an MRA. Breathing during the MRA acquisition will degrade the clarity of distal visceral vessels. The angiographic images of CTA may simultaneously provide adequate parenchymal assessment of the liver and bowel, as opposed to MRA in which additional time-consuming MRI sequences must be acquired to visualize those organs. CT is generally better than MRI in the visualization of the bowel wall for ischemia or malignancy. MRI is advantageous for locating tumors within the cirrhotic liver, or for discerning pancreatic masses.6 CT may be used to assess metallic intravascular stents for restenosis. Although metallic stents do not pose a hazard in MR, these devices are impenetrable by the electromagnetic signal of MR. MR provides a 3-dimensional view of the biliary structures through the acquisition of magnetic resonance cholangiopancreatography (MRCP).7 VOLUME 55, NO. 7 (SUPPL), 2002
MR angiography
C Anderson
MRA TECHNIQUE As described above, MRA may be performed using a variety of MR methods. In the abdomen, these include 2-dimensional TOF (2D-TOF), PC, and CEMRA. The first and second techniques are completely noninvasive and rely on the motion of blood to generate a bright vascular signal, whereas the third technique is more like CTA in that it uses a bolus injection of gadolinium contrast agent in an arm vein to cause bright intravascular signal.
A
2D-TOF The 2D-TOF8 (Fig. 1) is acquired as a series of thin sections, one at a time, and each during a separate breath hold. Blood that enters the section during each acquisition brings bright signal into the slice, whereas tissue that remains in the slice becomes dark. Therefore, it could be said that TOF is an image of inflow. The study may be interpreted from individual sections, or the sections may be stacked up and projected to form an angiogram. The 2D-TOF is ideal for quickly assessing a single vessel, but the technique is laborious when applied to the entire abdomen and pelvis. Typical applications for 2D-TOF include the determination of the patency of the portal or splenic vein (Fig. 1A and B) and the detection of intraluminal tumor or deep venous thrombosis (Fig. 1C). Although 2D-TOF provides an excellent evaluation of veins, it is rarely used for the study of the aorta and has been replaced by CEMRA for imaging of aortic branch vessels.
B
Phase-contrast imaging PC is a velocity-encoded method that may be used to measure mesenteric9 and portal blood flow or to generate an angiogram.10 PC imaging was once used extensively for portal venous studies, but like 2DTOF, it has been largely replaced by CEMRA. The disadvantage of phase contrast is that blood signal may not be uniform, but rather it reflects local blood flow patterns. Signal is lost in areas of flow disturbances, resulting in the appearance of a false stenosis. CEMRA CEMRA11 (Fig. 2) is similar in principle to CTA and was inspired by it. In this technique, multiple thin sections are rapidly acquired during the first pass of contrast agent after peripheral venous injection. An initial acquisition shows arterial structures. The acquisition may then be repeated several seconds later to demonstrate venous structures. In a seeming paradox, the faster the CEMRA acquisition, the better the contrast-to-noise ratio. This is because contrast agent may be injected more quickly, forming a more concentrated bolus, when the acquisition time is brief. VOLUME 55, NO. 7 (SUPPL), 2002
C Figure 1. Studies of the portal vein by 2D-TOF. A, Transaxial sections of upper abdomen of patient with chronic pancreatitis have been combined in a superoinferior projection to demonstrate the absence of the main portal vein and the presence of numerous small portoportal collaterals seen as bright curvilinear structures (arrows) in the porta hepatis. B, Transaxial section through liver in patient with hepatocellular carcinoma shows occlusion of left portal vein surrounded by cavernous transformation seen as a ring of bright dots (arrows). C, Patient with malignant thrombosis of the portal vein has filling defect (arrow) within the bright venous blood signal.
The study is performed during a breath hold. The typical breath hold requirement is 15 seconds or less, which most patients readily achieve. Patients with respiratory compromise, or who are unresponsive to commands, will not yield interpretable images of smaller vessels. IMAGE POSTPROCESSING AND INTERPRETATION Image postprocessing is an important aspect of CTA, but less so of MRA. In MRA, the brightest GASTROINTESTINAL ENDOSCOPY
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Figure 2. CEMRA of the normal mesenteric vessels, with visualization of colonic branches (arrow) of the superior mesenteric artery. The angiogram has been rendered with shading based on surface and depth information. (Image proved by Dr. Paul Finn, Northwestern University, and rendered on Siemens Leonardo workstation.)
objects in the image are vascular. Therefore, it is not necessary to remove other tissues from the acquired sections before generating a computer-rendered projection. The study may be interpreted from the original acquired “source” sections. Reformations, projections, and surface renderings may assist in the interpretation. Turbulent motion within a critical stenosis may cause signal loss on the MRA, and this in turn might result in an overestimation of the degree of stenosis. This phenomenon may be minimized by the practice of interpretation from source images rather than from projections, because residual signal is more visible on source images. Another advantage of source images is that the arterial wall and plaque may be visualized directly, further confirming the diagnosis. APPLICATIONS OF MRA IN THE ABDOMEN The common applications of MRA in the abdomen are the study of the aorta for occlusive disease, aneurysmal disease, or dissection, the study of the S44
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MR angiography
Figure 3. CEMRA of left renal artery stenosis (arrow) in an anteroposterior projection.
renal arteries for proximal occlusive disease (Fig. 3), and identification of accessory arteries, and the study of the portal venous system for thrombosis and collateral pathways of flow. The accuracy of MRA for these indications has been validated in comparison with conventional angiography.11-14 The use of MRA for the study of mesenteric arteries is relatively uncommon, perhaps reflecting the rare occurrence of mesenteric vascular diseases. PORTAL VENOUS IMAGING One of the first applications of MRA was abdominal venography using the 2D-TOF technique.15 Approximately 20 sections in the coronal or transaxial plane can be acquired of the liver in a few minutes. The resulting images are effective in defining venous and arterial anatomy, including patency and sites of portosystemic shunting.5 Bland intravascular thrombus may be differentiated from malignant thrombus by the presence of dark hemoglobin products (in the case of bland thrombus) or by enhancement when gadolinium is subsequently injected (in the case of malignant thrombus). The 2D-TOF may be used to define vascular anatomy in preparation for a TIPS intervention.16 VOLUME 55, NO. 7 (SUPPL), 2002
MR angiography
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C Anderson
B
Figure 4. Studies of the mesenteric arteries by CEMRA. A, Celiac artery stenosis (arrow) seen on left posterior oblique projection. Incidental finding in patient with rising creatinine. B, Patient who presented with sensation of dull fullness, nausea, and vomiting 30 to 60 minutes after meal. A lateral projection shows occlusion of the proximal celiac and superior mesenteric arteries (arrows) consistent with chronic mesenteric ischemia.
Flow direction of the portal vein may be determined by the use of saturation bands,15 or the flow velocity may be measured by PC.17 More recent publications have shown the advantages of CEMRA for abdominal venography.18,19 For example, Kreft et al.20 studied 36 patients with portal hypertension by conventional angiography and by CEMRA. CEMRA had an overall 100% sensitivity and 98% specificity for detection of the 42 splenic, portal, or superior mesenteric veins that were thrombosed on conventional angiography. LIVER TRANSPLANTATION MRA is an accepted method for both the planning and surveillance of liver transplants. Presurgically, the method is used to identify anatomic variants, such as a replaced right hepatic artery.10,21 PostVOLUME 55, NO. 7 (SUPPL), 2002
surgically, MRA is used to identify anastomotic strictures or venous thrombosis.22 An advantage of this technique is that arteries, veins, and varices may be opacified by contrast material regardless of the direction of blood flow and without the need for selective catheter injections as would be required by conventional angiography. CHRONIC MESENTERIC ISCHEMIA (CMI) The radiographic diagnosis of CMI is suggested by the presence of stenosis of at least 2 of the 3 mesenteric vessels—the celiac trunk, the superior mesenteric artery (SMA), and the inferior mesenteric artery (IMA). Many routes of collateral flow are available to the colon; therefore, the radiologic finding of a single stenosis might not be significant. The anatomic diagnosis must be correlated with presence GASTROINTESTINAL ENDOSCOPY
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MR angiography
of symptoms such as postprandial pain. Stenoses usually occur at the origin of the vessels and are readily demonstrated on CEMRA (Fig. 4).23-25 Holland et al.26 compared CEMRA with conventional angiography and found that CEMRA correctly identified 20 of 20 mesenteric artery stenoses, as well as 3 of 3 arcs of Riolan. Each of these lesions was at or near the origin of the vessel. Meaney et al.27 studied 14 patients by CEMRA and by conventional angiography, with identification of 22 of 24 significant proximal stenoses. Detection of more distal lesions is less reliable by CEMRA. Shirkhoda et al.28 examined 16 individuals and noted that 75% of first-order SMA branches, 60% of second-order branches, and just 50% of third-order branches were well depicted. The IMA was seen clearly in only 25% of studies. MR BLOOD FLOW STUDIES After a meal, blood flow is increased to normal mesenteric arteries. In CMI, however, postprandial augmentation of flow is greatly reduced. Furthermore, the degree of oxygenation of the superior mesenteric vein (SMV) may fall. This phenomenon may be used to improve the specificity of the MR diagnosis, because MR is capable of measuring both blood flow velocities and blood oxygenation in vivo. Li et al.29 applied PC to measure mesenteric flow rates as a function of time after a meal. They found the greatest differences between healthy volunteers and patients with CMI at 30 minutes. In a subsequent study,30 they noted the ratio of SMV to SMA flow decreased with the severity of SMA stenosis. Burkart et al.31 undertook confirmatory studies of mesenteric blood flow rates in patients with CMI using cine phase-contrast MR sequences. They, too, were able to detect a reduction in postprandial blood flow augmentation in comparison with normal controls. Furthermore, the ratio of SMA flow to SMV flow decreased in patients with significant mesenteric stenosis after a meal. The authors suggested that postprandial SMA flow or SMA/SMV flow ratios could be used to diagnose CMI. An interesting use of postprandial flow augmentation is to improve the quality of hepatic artery MRA. Kopka et al.32 used this phenomenon to show that MRA could replace conventional angiography in the evaluation of the hepatic arterial supply. Sugano et al.33 made novel use of MR blood flow measurements in a study of esophageal bleeding. Noting that esophageal bleeding occurs most often at night, they measured azygous and portal vein velocities throughout the day and found that maximum flow occurred at midnight. The administration of propranolol significantly reduced nighttime venous blood flow, which might reduce the incidence of bleeding. S46
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MR BLOOD OXIMETRY Oxyhemoglobin and deoxyhemoglobin have very different paramagnetic characteristics. As a result, oxygenated blood is much brighter on T2weighted sequences than is deoxygenated blood. This brightness may be calibrated and used to measure oxygen saturation and extraction of oxygen by tissues. Li et al.34 applied MR oximetry to patients with CMI and demonstrated a drop in SMV oxygen saturation. They proposed this measurement might provide a diagnostic test for CMI. ACUTE MESENTERIC ISCHEMIA Segmental small bowel ischemia has been induced in a porcine model with subsequent imaging by MRA and MR oximetry.35 In these studies, SMV oxygenation dropped significantly, in comparison both with the preischemia SMV and with the postischemia inferior vena cava (IVC). There was no statistical difference in the ability of CEMRA and conventional angiography to localize the ischemic segments. Although MR may be capable of diagnosing acute mesenteric ischemia, it is unlikely this method will enjoy widespread use. Acute intestinal ischemia requires expedited treatment. Once the diagnosis of acute ischemia is suspected, patients may undergo CT or proceed directly to the surgical suite. GI BLEEDING STUDIES The immediate role of conventional angiography in the actively bleeding patient is to locate the arterial source of hemorrhage, and to then to stop the bleeding by embolization of the feeding artery. MRA lacks sufficient resolution to visualize hemorrhage from small vessels, such as those in angiodysplasia, directly. But it might help locate the bowel segment that contains the bleeding vessel by using a technique similar in principle to radionuclide-labeled red blood cell scintigraphy. This is accomplished by use of new blood pool MR contrast agents that reside in the intravascular space for many hours. Extravasation of the agent into bowel may then be detected on MRI. The technique has been demonstrated in pigs.36 Routine use of these agents in human beings awaits FDA clearance of these experimental contrast agents. There are few published examples of the application of MRI or MRA to the acute phase of GI bleeding; however, Chevallier et al.37 reported a case in which ascending colonic varices were diagnosed by MRA. After TIPS and embolization, serial MRA was then used to demonstrate resolution of colonic varices and to surveil for their recurrence. VOLUME 55, NO. 7 (SUPPL), 2002
MR angiography
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CONCLUSIONS MRA is an effective method of arteriography and venography in the abdomen. It is an excellent alternative to Doppler ultrasound for hepatic vascular imaging when bowel gas or liver echogenicity precludes an acoustic window. It is a safe alternative to CTA in the patient who cannot receive iodinated contrast material as a result of compromised renal function. Together, MRA, MRI, and MRCP provide a comprehensive examination of many GI disorders. MRA is not equally adept at all vascular applications, however. It does not have sufficient resolution or immunity from motion to visualize small distal vessels, especially of the bowel.
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17. 18.
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REFERENCES 1. Laub GA, Kaiser WA. MR angiography with gradient motion refocusing. J Comput Assist Tomogr 1988;12:377-82. 2. Dumoulin CL, Hart HJ. Magnetic resonance angiography. Radiology 1986;161:717-20. 3. Prince MR, Yucel EK, Kaufman JA, Harrison DC, Geller DC. Dynamic gadolinium-enhanced 3D abdominal MR arteriography. J Magn Reson Imaging 1993;3:877-81. 4. Grist TM. MRA of the abdominal aorta and lower extremities. J Magn Reson Imaging 2000;11:32-43. 5. Finn JP, Kane RA, Edelman RR, Jenkins RL, Lewis WD, Muller M, et al. Imaging of the portal venous system in patients with cirrhosis: MR angiography vs duplex Doppler sonography. AJR Am J Roentgenol 1993;161:989-94. 6. Catalano C, Pavone P, Laghi A, Panebianco V, Scipioni A, Fanelli F, et al. Pancreatic adenocarcinoma: combination of MR imaging, MR angiography and MR cholangiopancreatography for the diagnosis and assessment of respectability. Eur Radiol 1998;8:428-34. 7. Wallner BK, Schumacher KA, Weidenmaier W. Dilated biliary tract: evaluation with MR cholangiography with a T2-weighted contrast-enhanced fast sequence. Radiology 1991;181:805-8. 8. Keller PJ, Drayer BP, Fram EK, Williams KD, Dumoulin CL, Souza SP. MR angiography with two-dimensional acquisition and three-dimensional display. Radiology 1989;173:527-32. 9. Wasser MN, Geelkerken RH, Kouwenhoven M, van Bockel JH, Hermans J, Schultze Kool LJ, et al. Systolically gated phase-contrast MRA of mesenteric arteries in suspected mesenteric ischemia. J Comput Assist Tomogr 1996;20:262-8. 10. Nghiem HV, Freeny PC, Winter TC, Mack LA, Yuan C. Phasecontrast MR angiography of the portal venous system: preoperative findings in liver transplant recipients. AJR Am J Roentgenol 1994;163:445-50. 11. Prince MR, Narasimham DL, Stanley JC, Chenevert TL, Williams DM, Marx MV, et al. Breath-hold gadoliniumenhanced MR angiography of the abdominal aorta and its major branches. Radiology 1995;197:785-92. 12. Snidow JJ, Johnson MS, Harris VJ, Margosian Pm, Aisen AM, Lalka SG, et al. Three-dimensional gadolinium-enhanced MR angiography for aorto-iliac inflow assessment plus renal artery screening in a single breath hold. Radiology 1996;198: 725-32. 13. Bakker J, Beek FJ, Beutler JJ, Hene RJ, de Kort GA, de Lange EE, et al. Renal artery stenosis and accessory renal arteries: accuracy of detection and visualization with gadoliniumenhance breath hold R angiography. Radiology 1998;207:497504. 14. Hany TF, Leung DA, Pfammatter T, Debatin JF. ContrastVOLUME 55, NO. 7 (SUPPL), 2002
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enhanced magnetic resonance angiography of the renal arteries. Invest Radiol 1998;33:653-9. Edelman RR, Zhao B, Liu C, Wentz KU, Mattle HP, Finn JP, et al. MR angiography and dynamic flow evaluation of the portal venous system. AJR Am J Roentgenol 1989;153:755-60. Eustace S, Buff B, Kruskal J, Roizental M, Finn FP, Longmaid HE, et al. Magnetic resonance angiography in transjugular intrahepatic portosystemic stenting: comparison with contrast hepatic and portal venography. Eur J Radiol 1994;19:43-9. Debatin JF. MR quantification of flow in abdominal vessels. Abdom Imaging 1998;23:485-95. Rogers PM, Ward J, Baudouin CJ, Ridgway JP, Robinson PJ. Dynamic contrast-enhanced MR imaging of the portal venous system: comparison with x-ray angiography. Radiology 1994;191:741-5. Leyendecker JR, Rivera E, Washburn WK, Johnson SP, Diffin DC, Eason JD. MR angiography of the portal venous system: techniques, interpretation, and clinical applications. Radiographics 1997;17;1425-43. Kreft B, Strunk H, Flacke S, Wolff M, Conrad R, Gieseke J, et al. Detection of thrombosis in the portal venous system: comparison of contrast-enhanced MR angiography with intraarterial digital subtraction angiography. Radiology 2000;216: 86-92. Finn JP, Edelman RR, Jenkins RL, Lewis WD, Longmaid HE, Kane RA, et al. Liver transplantation: MR angiography with surgical validation. Radiology 1991;179:265-9. Stafford-Johnson DB, Hamilton BH, Dong Q, Cho KJ, Turcotte JG, Fontana RJ, et al. Vascular complications of liver transplantation: evaluation with gadolinium-enhanced MR angiography. Radiology 1998;207:153-60. Meaney JFM. Non-invasive evaluation of the visceral arteries with magnetic resonance angiography. Eur Radiol 1999;9: 1267-76. Baden JG, Douglas JR, Grist TM. Contrast-enhanced threedimensional magnetic resonance angiography of the mesenteric vasculature. J Magn Reson Imaging 1999;10:369-75. Shirkhoda A, Konez O, Shetty AN, et al. Contrast enhanced MR angiography of the mesenteric circulation: a pictorial essay. Radiographics 1998:18;851-61. Holland GA, Dougherty L, Carpenter JP, Golden MA, Gilfeather M, Slossman F, et al. Breath-hold ultrafast threedimensional MR angiography of the aorta and the renal and other visceral abdominal arteries. AJR Am J Roentgenol 1996;166:971-81. Meaney JFM, Prince MR, Nostrand TT, et al. Gadoliniumenhanced magnetic resonance angiography in patients with suspected chronic mesenteric insufficiency. J Magn Reson Imaging 1997;7:171-6. Shirkhoda A, Konez O, Shetty AN, Bis KG, Ellwood RA, Kirsch MJ, et al. Mesenteric circulation: three-dimensional MR angiography with a gadolinium-enhanced multiecho gradient-echo technique. Radiology 1997;202:257-61. Li KCP, Whitney WS, McDonnel C, et al. Chronic mesenteric ischemia: evaluation with phase-contrast cine imaging. Radiology 1994;190:175-9. Li KCP, Hopkins KL, Dalman RL, Song CK. Simultaneous measurement of flow in the superior mesenteric vein and artery with cine phase-contrast MR imaging: value in diagnosis of chronic mesenteric ischemia. Radiology 1995;194:327-30. Burkart DJ, Johnson CD, Reading CC, Ehman RL. MR measurements of mesenteric venous flow: prospective evaluation in healthy volunteers and patients with chronic mesenteric ischemia. Radiology 1995;194:801-6. GASTROINTESTINAL ENDOSCOPY
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32. Kopka L, Radenwaldt J, Vosshenrich R, et al. Hepatic blood supply: comparison of optimized dual phase contrastenhanced three-dimensional MR angiography and digital subtraction angiography. Radiology 1999;211:51-8. 33. Sugano S, Yamamoto K, Ishii K Watanabe M, Tanikawa K. Daily variation of azygous and portal blood flow and the effect of propranolol administration once an evening in cirrhotics. J Hepatol 2001;34:26-31. 34. Li KC, Dalman RL, Ch’en IY, Pelc LR, Song CK, Moon WK, et al. Chronic mesenteric ischemia: use of in vivo MR imaging measurements of blood oxygen saturation in the superior mesenteric vein for diagnosis. Radiology 1997;204:71-7. 35. Chan FP, Li KC, Heiss SG, Razavi MK. A comprehensive
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approach using MR imaging to diagnose acute segmental mesenteric ischemia in a porcine model. AJR Am J Roentgenol 1999;173:523-9. 36. Hilfiker PR, Weishaupt D, Kacl GM, Hetzer FH, Griff MD, Ruehm SG, et al. Comparison of three-dimensional magnetic resonance imaging in conjunction with a blood pool contrast agent and nuclear scintigraphy for detection of experimentally induced gastrointestinal bleeding. Gut 1999;45:581-7. 37. Chevallier P, Motamedi JP, Demuth N, Caroli-Bose FX, Oddo F, Padovani B. Ascending colonic variceal bleeding: utility of phase-contrast MR and portography in diagnosis and followup after treatment with TIPS and variceal embolization. Eur Radiol 2000;10:1280-3.
VOLUME 55, NO. 7 (SUPPL), 2002
MRA is a type of magnetic resonance imaging (MRI) in which blood appears bright. To form a magnetic resonance (MR) angiogram, a 3-dimensional set of thin sections is acquired through the region of interest. The images are then processed by computer to create a 2-dimensional projected display that resembles a conventional angiogram. There are many ways to cause blood to appear bright on MRI. Each of these mechanisms corresponds to a different type of MRA. Brightness may result from the entry of blood into the section. This mechanism is responsible for the time-of-flight (TOF) methods.1 Brightness may be dependent on the velocity of blood, which is the principle behind phase-contrast (PC) MRA.2 Brightness may result from the injection of contrast agents, which is the basis for contrast-enhanced MRA (CEMRA).3 Other mechanisms exist as well, although they are much less common than these three. In recent years, CEMRA has emerged as the dominant MRA method. CEMRA is applicable to nearly every abdominal vessel, including the aorta, renal arteries, mesenteric arteries, and portal vein.4 CEMRA is much faster than TOF and PC. It is accomplished in a single breath hold and so is less exhausting to the patient, as compared with TOF, which may require a separate breath hold for each section. CEMRA is demonstrably better than TOF or PC in the imaging of arterial branch vessels. Furthermore, it resembles conventional angiography and CT angiography (CTA), both of which use the same principle of blood enhancement by intravascular contrast agents. NONINVASIVE VASCULAR IMAGING Vascular imaging of the abdomen was once the exclusive domain of catheter angiography, but is now performed more safely and cheaply by noninvasive Doppler ultrasound (DUS), MRA, or CTA. Each of these noninvasive modalities has its own strengths and favored applications. From the San Francisco VA Medical Center, San Francisco, California. Reprint requests to: Charles M. Anderson, MD, PhD, Radiology (114), SFVAMC, 4150 Clement St, San Francisco, CA 94121. 37/0/124744 doi:10.1067/mge.2002.124744 S42
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DUS is the first choice for liver vessel imaging, particularly when measurement of velocity and direction of flow is required. Velocities are used to evaluate of portal hypertension and to assess the function of transjugular intrahepatic portosystemic shunts (TIPS). Ultrasound plays a limited role in splanchnic vessel imaging as a result of overlying bowel gas, which impedes the acoustic signal.5 MRA and CTA provide rapid 3-dimensional angiograms of the aorta and its proximal mesenteric branches, as well as of the portosplenic veins and varices. In most cases, MRA and CTA provide equivalent vascular information. The choice of using MRA or CTA is usually based on imaging considerations other than vascular. For example: Unlike CTA, MRA does not use iodinated contrast, and so is indicated for patients with renal insufficiency or who have an allergy to iodinated contrast preparations. Iodinated contrast is also undesirable in the event that an interventional procedure must be performed on the same day, for example to embolize a bleeding artery, because the intervention will also require the injection of iodinated contrast material. CTA allows open access to the critically ill patient who may require close physiological monitoring. In MRA, physical access to the patient within the bore of the magnet is limited. In addition, the critically ill patient may not be able to hold his or her breath for the approximately 15 seconds required to perform an MRA. Breathing during the MRA acquisition will degrade the clarity of distal visceral vessels. The angiographic images of CTA may simultaneously provide adequate parenchymal assessment of the liver and bowel, as opposed to MRA in which additional time-consuming MRI sequences must be acquired to visualize those organs. CT is generally better than MRI in the visualization of the bowel wall for ischemia or malignancy. MRI is advantageous for locating tumors within the cirrhotic liver, or for discerning pancreatic masses.6 CT may be used to assess metallic intravascular stents for restenosis. Although metallic stents do not pose a hazard in MR, these devices are impenetrable by the electromagnetic signal of MR. MR provides a 3-dimensional view of the biliary structures through the acquisition of magnetic resonance cholangiopancreatography (MRCP).7 VOLUME 55, NO. 7 (SUPPL), 2002
MR angiography
C Anderson
MRA TECHNIQUE As described above, MRA may be performed using a variety of MR methods. In the abdomen, these include 2-dimensional TOF (2D-TOF), PC, and CEMRA. The first and second techniques are completely noninvasive and rely on the motion of blood to generate a bright vascular signal, whereas the third technique is more like CTA in that it uses a bolus injection of gadolinium contrast agent in an arm vein to cause bright intravascular signal.
A
2D-TOF The 2D-TOF8 (Fig. 1) is acquired as a series of thin sections, one at a time, and each during a separate breath hold. Blood that enters the section during each acquisition brings bright signal into the slice, whereas tissue that remains in the slice becomes dark. Therefore, it could be said that TOF is an image of inflow. The study may be interpreted from individual sections, or the sections may be stacked up and projected to form an angiogram. The 2D-TOF is ideal for quickly assessing a single vessel, but the technique is laborious when applied to the entire abdomen and pelvis. Typical applications for 2D-TOF include the determination of the patency of the portal or splenic vein (Fig. 1A and B) and the detection of intraluminal tumor or deep venous thrombosis (Fig. 1C). Although 2D-TOF provides an excellent evaluation of veins, it is rarely used for the study of the aorta and has been replaced by CEMRA for imaging of aortic branch vessels.
B
Phase-contrast imaging PC is a velocity-encoded method that may be used to measure mesenteric9 and portal blood flow or to generate an angiogram.10 PC imaging was once used extensively for portal venous studies, but like 2DTOF, it has been largely replaced by CEMRA. The disadvantage of phase contrast is that blood signal may not be uniform, but rather it reflects local blood flow patterns. Signal is lost in areas of flow disturbances, resulting in the appearance of a false stenosis. CEMRA CEMRA11 (Fig. 2) is similar in principle to CTA and was inspired by it. In this technique, multiple thin sections are rapidly acquired during the first pass of contrast agent after peripheral venous injection. An initial acquisition shows arterial structures. The acquisition may then be repeated several seconds later to demonstrate venous structures. In a seeming paradox, the faster the CEMRA acquisition, the better the contrast-to-noise ratio. This is because contrast agent may be injected more quickly, forming a more concentrated bolus, when the acquisition time is brief. VOLUME 55, NO. 7 (SUPPL), 2002
C Figure 1. Studies of the portal vein by 2D-TOF. A, Transaxial sections of upper abdomen of patient with chronic pancreatitis have been combined in a superoinferior projection to demonstrate the absence of the main portal vein and the presence of numerous small portoportal collaterals seen as bright curvilinear structures (arrows) in the porta hepatis. B, Transaxial section through liver in patient with hepatocellular carcinoma shows occlusion of left portal vein surrounded by cavernous transformation seen as a ring of bright dots (arrows). C, Patient with malignant thrombosis of the portal vein has filling defect (arrow) within the bright venous blood signal.
The study is performed during a breath hold. The typical breath hold requirement is 15 seconds or less, which most patients readily achieve. Patients with respiratory compromise, or who are unresponsive to commands, will not yield interpretable images of smaller vessels. IMAGE POSTPROCESSING AND INTERPRETATION Image postprocessing is an important aspect of CTA, but less so of MRA. In MRA, the brightest GASTROINTESTINAL ENDOSCOPY
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Figure 2. CEMRA of the normal mesenteric vessels, with visualization of colonic branches (arrow) of the superior mesenteric artery. The angiogram has been rendered with shading based on surface and depth information. (Image proved by Dr. Paul Finn, Northwestern University, and rendered on Siemens Leonardo workstation.)
objects in the image are vascular. Therefore, it is not necessary to remove other tissues from the acquired sections before generating a computer-rendered projection. The study may be interpreted from the original acquired “source” sections. Reformations, projections, and surface renderings may assist in the interpretation. Turbulent motion within a critical stenosis may cause signal loss on the MRA, and this in turn might result in an overestimation of the degree of stenosis. This phenomenon may be minimized by the practice of interpretation from source images rather than from projections, because residual signal is more visible on source images. Another advantage of source images is that the arterial wall and plaque may be visualized directly, further confirming the diagnosis. APPLICATIONS OF MRA IN THE ABDOMEN The common applications of MRA in the abdomen are the study of the aorta for occlusive disease, aneurysmal disease, or dissection, the study of the S44
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Figure 3. CEMRA of left renal artery stenosis (arrow) in an anteroposterior projection.
renal arteries for proximal occlusive disease (Fig. 3), and identification of accessory arteries, and the study of the portal venous system for thrombosis and collateral pathways of flow. The accuracy of MRA for these indications has been validated in comparison with conventional angiography.11-14 The use of MRA for the study of mesenteric arteries is relatively uncommon, perhaps reflecting the rare occurrence of mesenteric vascular diseases. PORTAL VENOUS IMAGING One of the first applications of MRA was abdominal venography using the 2D-TOF technique.15 Approximately 20 sections in the coronal or transaxial plane can be acquired of the liver in a few minutes. The resulting images are effective in defining venous and arterial anatomy, including patency and sites of portosystemic shunting.5 Bland intravascular thrombus may be differentiated from malignant thrombus by the presence of dark hemoglobin products (in the case of bland thrombus) or by enhancement when gadolinium is subsequently injected (in the case of malignant thrombus). The 2D-TOF may be used to define vascular anatomy in preparation for a TIPS intervention.16 VOLUME 55, NO. 7 (SUPPL), 2002
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Figure 4. Studies of the mesenteric arteries by CEMRA. A, Celiac artery stenosis (arrow) seen on left posterior oblique projection. Incidental finding in patient with rising creatinine. B, Patient who presented with sensation of dull fullness, nausea, and vomiting 30 to 60 minutes after meal. A lateral projection shows occlusion of the proximal celiac and superior mesenteric arteries (arrows) consistent with chronic mesenteric ischemia.
Flow direction of the portal vein may be determined by the use of saturation bands,15 or the flow velocity may be measured by PC.17 More recent publications have shown the advantages of CEMRA for abdominal venography.18,19 For example, Kreft et al.20 studied 36 patients with portal hypertension by conventional angiography and by CEMRA. CEMRA had an overall 100% sensitivity and 98% specificity for detection of the 42 splenic, portal, or superior mesenteric veins that were thrombosed on conventional angiography. LIVER TRANSPLANTATION MRA is an accepted method for both the planning and surveillance of liver transplants. Presurgically, the method is used to identify anatomic variants, such as a replaced right hepatic artery.10,21 PostVOLUME 55, NO. 7 (SUPPL), 2002
surgically, MRA is used to identify anastomotic strictures or venous thrombosis.22 An advantage of this technique is that arteries, veins, and varices may be opacified by contrast material regardless of the direction of blood flow and without the need for selective catheter injections as would be required by conventional angiography. CHRONIC MESENTERIC ISCHEMIA (CMI) The radiographic diagnosis of CMI is suggested by the presence of stenosis of at least 2 of the 3 mesenteric vessels—the celiac trunk, the superior mesenteric artery (SMA), and the inferior mesenteric artery (IMA). Many routes of collateral flow are available to the colon; therefore, the radiologic finding of a single stenosis might not be significant. The anatomic diagnosis must be correlated with presence GASTROINTESTINAL ENDOSCOPY
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of symptoms such as postprandial pain. Stenoses usually occur at the origin of the vessels and are readily demonstrated on CEMRA (Fig. 4).23-25 Holland et al.26 compared CEMRA with conventional angiography and found that CEMRA correctly identified 20 of 20 mesenteric artery stenoses, as well as 3 of 3 arcs of Riolan. Each of these lesions was at or near the origin of the vessel. Meaney et al.27 studied 14 patients by CEMRA and by conventional angiography, with identification of 22 of 24 significant proximal stenoses. Detection of more distal lesions is less reliable by CEMRA. Shirkhoda et al.28 examined 16 individuals and noted that 75% of first-order SMA branches, 60% of second-order branches, and just 50% of third-order branches were well depicted. The IMA was seen clearly in only 25% of studies. MR BLOOD FLOW STUDIES After a meal, blood flow is increased to normal mesenteric arteries. In CMI, however, postprandial augmentation of flow is greatly reduced. Furthermore, the degree of oxygenation of the superior mesenteric vein (SMV) may fall. This phenomenon may be used to improve the specificity of the MR diagnosis, because MR is capable of measuring both blood flow velocities and blood oxygenation in vivo. Li et al.29 applied PC to measure mesenteric flow rates as a function of time after a meal. They found the greatest differences between healthy volunteers and patients with CMI at 30 minutes. In a subsequent study,30 they noted the ratio of SMV to SMA flow decreased with the severity of SMA stenosis. Burkart et al.31 undertook confirmatory studies of mesenteric blood flow rates in patients with CMI using cine phase-contrast MR sequences. They, too, were able to detect a reduction in postprandial blood flow augmentation in comparison with normal controls. Furthermore, the ratio of SMA flow to SMV flow decreased in patients with significant mesenteric stenosis after a meal. The authors suggested that postprandial SMA flow or SMA/SMV flow ratios could be used to diagnose CMI. An interesting use of postprandial flow augmentation is to improve the quality of hepatic artery MRA. Kopka et al.32 used this phenomenon to show that MRA could replace conventional angiography in the evaluation of the hepatic arterial supply. Sugano et al.33 made novel use of MR blood flow measurements in a study of esophageal bleeding. Noting that esophageal bleeding occurs most often at night, they measured azygous and portal vein velocities throughout the day and found that maximum flow occurred at midnight. The administration of propranolol significantly reduced nighttime venous blood flow, which might reduce the incidence of bleeding. S46
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MR BLOOD OXIMETRY Oxyhemoglobin and deoxyhemoglobin have very different paramagnetic characteristics. As a result, oxygenated blood is much brighter on T2weighted sequences than is deoxygenated blood. This brightness may be calibrated and used to measure oxygen saturation and extraction of oxygen by tissues. Li et al.34 applied MR oximetry to patients with CMI and demonstrated a drop in SMV oxygen saturation. They proposed this measurement might provide a diagnostic test for CMI. ACUTE MESENTERIC ISCHEMIA Segmental small bowel ischemia has been induced in a porcine model with subsequent imaging by MRA and MR oximetry.35 In these studies, SMV oxygenation dropped significantly, in comparison both with the preischemia SMV and with the postischemia inferior vena cava (IVC). There was no statistical difference in the ability of CEMRA and conventional angiography to localize the ischemic segments. Although MR may be capable of diagnosing acute mesenteric ischemia, it is unlikely this method will enjoy widespread use. Acute intestinal ischemia requires expedited treatment. Once the diagnosis of acute ischemia is suspected, patients may undergo CT or proceed directly to the surgical suite. GI BLEEDING STUDIES The immediate role of conventional angiography in the actively bleeding patient is to locate the arterial source of hemorrhage, and to then to stop the bleeding by embolization of the feeding artery. MRA lacks sufficient resolution to visualize hemorrhage from small vessels, such as those in angiodysplasia, directly. But it might help locate the bowel segment that contains the bleeding vessel by using a technique similar in principle to radionuclide-labeled red blood cell scintigraphy. This is accomplished by use of new blood pool MR contrast agents that reside in the intravascular space for many hours. Extravasation of the agent into bowel may then be detected on MRI. The technique has been demonstrated in pigs.36 Routine use of these agents in human beings awaits FDA clearance of these experimental contrast agents. There are few published examples of the application of MRI or MRA to the acute phase of GI bleeding; however, Chevallier et al.37 reported a case in which ascending colonic varices were diagnosed by MRA. After TIPS and embolization, serial MRA was then used to demonstrate resolution of colonic varices and to surveil for their recurrence. VOLUME 55, NO. 7 (SUPPL), 2002
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CONCLUSIONS MRA is an effective method of arteriography and venography in the abdomen. It is an excellent alternative to Doppler ultrasound for hepatic vascular imaging when bowel gas or liver echogenicity precludes an acoustic window. It is a safe alternative to CTA in the patient who cannot receive iodinated contrast material as a result of compromised renal function. Together, MRA, MRI, and MRCP provide a comprehensive examination of many GI disorders. MRA is not equally adept at all vascular applications, however. It does not have sufficient resolution or immunity from motion to visualize small distal vessels, especially of the bowel.
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32. Kopka L, Radenwaldt J, Vosshenrich R, et al. Hepatic blood supply: comparison of optimized dual phase contrastenhanced three-dimensional MR angiography and digital subtraction angiography. Radiology 1999;211:51-8. 33. Sugano S, Yamamoto K, Ishii K Watanabe M, Tanikawa K. Daily variation of azygous and portal blood flow and the effect of propranolol administration once an evening in cirrhotics. J Hepatol 2001;34:26-31. 34. Li KC, Dalman RL, Ch’en IY, Pelc LR, Song CK, Moon WK, et al. Chronic mesenteric ischemia: use of in vivo MR imaging measurements of blood oxygen saturation in the superior mesenteric vein for diagnosis. Radiology 1997;204:71-7. 35. Chan FP, Li KC, Heiss SG, Razavi MK. A comprehensive
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approach using MR imaging to diagnose acute segmental mesenteric ischemia in a porcine model. AJR Am J Roentgenol 1999;173:523-9. 36. Hilfiker PR, Weishaupt D, Kacl GM, Hetzer FH, Griff MD, Ruehm SG, et al. Comparison of three-dimensional magnetic resonance imaging in conjunction with a blood pool contrast agent and nuclear scintigraphy for detection of experimentally induced gastrointestinal bleeding. Gut 1999;45:581-7. 37. Chevallier P, Motamedi JP, Demuth N, Caroli-Bose FX, Oddo F, Padovani B. Ascending colonic variceal bleeding: utility of phase-contrast MR and portography in diagnosis and followup after treatment with TIPS and variceal embolization. Eur Radiol 2000;10:1280-3.
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