Review -- Magnetic Resonance Imaging of the Liver: How I Do It
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Ghislaine SURREL
maladies-lysosomales-subscribe@yahoogroupes.fr
Posted 04/28/2006
Richard C Semelka; Diego R Martin; N Cem Balci
The present paper provides a brief overview of the rationale behind magnetic resonance imaging (MRI) techniques, a description of the most common sequences used, and a general approach to performing liver MRI.
Fundamentals of Magnetic Resonance Imaging (MRI) Techniques Applied to the Liver. Image quality, reproducibility of image quality, and good conspicuity of disease requires the use of sequences that are robust and reliable and avoid artifacts.[1-5] Maximizing these principles to achieve high-quality diagnostic MR images usually requires the use of fast scanning techniques, with the overall intention of generating images with consistent image quality that demonstrate consistent display of disease processes. The important goal of shorter examination time may also be achieved with the same principles that maximize diagnostic quality. With the decrease of imaging times for individual sequences, a greater variety of sequences may be employed without increasing the total examination time. This approach contributes to one of the major strengths of MRI, which is comprehensive information on disease processes.
Respiration, bowel peristalsis and vascular pulsations are related to major artifacts that have lessened the reproducibility of MRI. Breathing-independent sequences and breath-hold sequences form the foundation of high-quality MRI studies of the abdomen.
Disease conspicuity depends on the principle of maximizing the difference in signal intensities between diseased tissues and the background tissue. For disease processes situated within or adjacent to fat, this is readily performed by manipulating the signal intensity of fat, which can range from low to high in signal intensity on both T1-weighted and T2-weighted images. For example, diseases that are low in signal intensity on T1-weighted images, such as peritoneal fluid or retroperitoneal fibrosis, are most conspicuous on T1-weighted sequences in which fat is high in signal intensity (i.e. sequences without fat suppression). Conversely, diseases that are high in signal intensity, such as subacute blood or proteinaceous fluid, are more conspicuous if fat is rendered low in signal intensity with the use of fat suppression techniques. On T2-weighted images, diseases that are low in signal intensity, such as fibrous tissue, are most conspicuous on sequences in which background fat is high in signal intensity, such as echo-train spin-echo sequences. Diseases that are moderate to high in signal intensity, such as lymphadenopathy or ascites, are most conspicuous on sequences in which fat signal intensity is low, such as fat-suppressed sequences.
Gadolinium chelate enhancement may be routinely useful because it provides at least two further imaging properties that facilitate detection and characterization of disease, specifically the pattern of blood delivery (i.e. capillary enhancement) and the size and/or rapidity of drainage of the interstitial space (i.e. interstitial enhancement).[6] Capillary-phase image acquisition is achieved by using a short-duration sequence initiated immediately after gadolinium injection. Spoiled gradient-echo (SGE) sequence, performed as multisection 2- or 3-dimensional acquisition, is an ideal sequence to use for capillary phase imaging. The majority of focal mass lesions are best evaluated in the capillary phase of enhancement, particularly lesions that do not distort the margins of the organs in which they are located (e.g. focal liver, spleen or pancreatic lesions). Images acquired 1.5–10 min after contrast administration are in the interstitial phase of enhancement with the optimal window being 2 to5 min post-contrast. Diseases that are superficial, spreading or inflammatory in nature are generally well shown on interstitial phase images. The concomitant use of fat suppression serves to increase the conspicuity of disease processes characterized by increased enhancement on interstitial phase images including peritoneal metastases, cholangiocarcinoma, ascending cholangitis, inflammatory bowel disease and abscesses.[7,8]
The great majority of diseases can be characterized by defining their appearance on T1, T2 and early and late postgadolinium images. Throughout this review the combination of these four parameters for the evaluation of liver disease will be stressed.
T1-weighted sequences are routinely useful for investigating diseases of the liver. The primary information that precontrast T1-weighted images provide includes: (i) information on abnormally increased fluid content or fibrous tissue content that appears low in signal intensity on T1-weighted images; and (ii) information on the presence of subacute blood or concentrated protein, which are both high in signal intensity. T1-weighted sequences obtained without fat suppression also demonstrate the presence of fat as high-signal intensity tissue. The routine use of an additional fat attenuating technique facilitates reliable characterization of fatty lesions.
Spoiled Gradient-echo Sequences. SGE sequences are the most important and versatile sequences for studying liver disease. These sequences provide T1-weighted imaging and, with the use of phased-array multicoil imaging, may be used to replace longer duration sequences such as the T1-weighted spin-echo (SE) sequence. Image parameters for SGE are: (i) relatively long repetition time (TR) (approximately 150 ms) to maximize signal-to-noise ratio and the number of sections that can be acquired in one multisection acquisition; and (ii) the shortest in-phase echo time (TE) (approximately 6.0 ms at 1.0 T and 4.2–4.5 ms at 1.5 T) to maximize signal-to-noise ratio and the number of sections per acquisition.2 Hydrogen protons in a voxel containing 100% fat will process approximately 220–230 Hz slower than a voxel comprised of 100% water, at 1.5 Tesla. That means every 4.4 ms the fat protons will lag behind by 360 degrees and regain in-phase orientation relative to water protons, while at 2.2 ms, or at half this time, the fat and water protons will be 180 degrees out-of-phase. Current generation MR control software have incorporated dual-echo breath-hold SGE sequences that can acquire two sets of k-space filled to obtain two sets of images, one set in-phase, the other out-of-phase, with spatially matched slices. For routine T1-weighted images, in-phase TE may be preferable to the shorter out-of-phase echo times (4.0 ms at 1.0 T and 2.2–2.4 ms at 1.5 T), to avoid both phase-cancellation artifact around the borders of organs and fat-water phase cancellation in tissues containing both fat and water protons. Flip angle should be approximately 70–90 degrees to maximize T1-weighted signal. With the use of the larger built-in body coil, the signal-to-noise ratio of SGE sequences is usually suboptimal with section thickness less than 8 mm, whereas with the phased-array surface coils, section thickness of 5 mm results in diagnostically adequate images. On new MRI machines, more than 22 sections may be acquired in a 20 s breath-hold, or 44 paired sections when using the dual echo technique.
Application of Out-of-phase Apoiled Gradient-echo. Out-of-phase (opposed-phase) SGE images are useful for demonstrating diseased tissue in which mixtures of fat and water protons are present within the same voxel. A voxel containing predominantly only fat, or only water, will not demonstrate diminished signal on out-of-phase images. A TE of 2.2 ms is advisable at 1.5 T, and 4.4 ms is advisable at 1.0 T. A TE of 6.6 ms is also out of phase at 1.5 T, but the shorter TE of 2.2 ms is preferable because of decreased susceptibility effects (i.e. the shorter echo time reduces the time for dephasing effects to accumulate, as is caused by metals or gas), more sections can be acquired per sequence acquisition, signal is higher, the sequence is more T1 weighted, and in combination with a T2-weighted sequence, it is easier to distinguish fat and iron in the liver. At 1.5T, both fat and iron cause liver signal decrease on out-of-phase images using a TE of 6.6 ms, relative to the in-phase images acquired with a TE of 4.4 ms, whereas on 2.2 ms out-of-phase TE images fat is darker and iron is brighter relative to TE 4 ms images (Fig. 1). Relative sensitivity to magnetic susceptibility effects, which increase with increases in TE, also can be used to distinguish iron-containing paramagnetic structures (e.g. surgical clips or foci of iron deposition in the spleen or liver) from non-magnetic signal void structures (e.g. calcium). To illustrate this point, the signal void susceptibility artifact from surgical clips increases in size as the TE increases from 2.2 to 4.4 ms, whereas the signal void from calcium remains unchanged. However, the most common indications for out-of-phase imaging are the detection of abnormal fat accumulation within the liver and the detection of lipid within adrenal masses, a feature used to characterize benign adrenal adenomas. As discussed previously, current MRI systems can acquire both in- and out-of-phase images during a single breath-hold SGE acquisition, and this feature should always be used on routine imaging of the abdomen.
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Figure 1. (click image to zoom) Axial T1-weighted (a) in phase and (b) out of phase images. The in phase image reveals a hypointense area in the left liver lobe (arrow). On the out of phase image, liver loses its signal except the fat sparing area in the left liver lobe (arrow). |
Intravascular Gadolinium-chelate Contrast Enhanced Spoiled Gradient-echo. In addition to its use as precontrast T1-weighted images, SGE should be routinely used for multiphase image acquisition after gadolinium administration for investigation of the liver.[2,6] An important feature of the multisection acquisition of SGE is that the central phase-encoding steps are generally used to fill central k-space, which determines image contrast. This contrast component of the dataset is acquired over a 4 to 5 s period for the entire data set, and is essentially shared by each individual section. Thus, the data acquisition is sufficiently short for the entire data set to isolate a distinct phase of enhancement (e.g. hepatic arterial dominant phase) (Fig. 2). Furthermore, this ensures that images of organs, such as the liver, are shown in the same phase of contrast enhancement uniformly throughout the volume of the tissue.
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Figure 2. (click image to zoom) Arterial phase spoiled gradient-echo (SGE) image (a) in a patient with hypervascular liver metastases (white arrows). Absence of contrast in hepatic veins is an indication of good timing (black arrow). The lesions fade in the late phase contrast enhanced images (b). |
Fat-suppressed Spoiled Gradient-echo Sequences. Fat-suppressed (FS) SGE sequences are routinely used as precontrast images for evaluating the pancreas and for the detection of subacute blood. Fat suppression is generally achieved on SGE images by selectively stimulating slower processing hydrogen protons associated with fat using a tuned radio-frequency (rf) pulse, followed by spoiler gradients, prior to performing the gradient echo imaging components of the sequence. Image parameters are similar to those for standard SGE. It may be advantageous to use a lower out-of-phase echo time (2.2–2.5 ms at 1.5 T), which benefits from additional fat-attenuating effects and also increases signal-to-noise ratio and the number of sections per acquisition. On current MRI machines fat-suppressed SGE may acquire 22 sections in a 20 s breath-hold with reproducible uniform fat suppression. One method modern systems use to reduce the amount of additional time fat suppression adds to the SGE sequence and acquires a greater number of slices per breath-hold, is to perform a fat suppression step only after several phase encoding steps, instead of after every phase encode. Another approach is to selectively tune the stimulation rf pulse to activate only protons in water, but not in fat, thus eliminating the need to add fat saturation pulses.
FS SGE images are used to improve the contrast between intra-abdominal fat and diseased tissues and blood vessels on interstitial-phase gadolinium-enhanced images (Fig. 3). Gadolinium enhancement generally increases the signal intensity of blood vessels and disease tissue, and fat suppression diminishes the competing high signal intensity of background fat (Fig. 4).
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Figure 3. (click image to zoom) T1-weighted fat suppressed spoiled gradient-echo (SGE) image reveals good delineation of the normal pancreatic head (arrow). |
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Figure 4. (click image to zoom) Multiple hepatocellular carcinoma (HCC) in a cirrhotic liver in (a) arterial phase spoiled gradient-echo (SGE) image (arrows); (b) the late phase postgadolinium image reveals the washout and better delineation of the lesions (arrows). |
Three-dimensional Gradient Echo. Three-dimensional (3-D) SGE imaging has been used extensively for MR angiography (MRA), but only recently has evolved into an accepted useful technique for imaging the liver.[1,5] This development has partly been achieved simply by reducing the flip angle from 70 to 90 degrees, used for angiography, down to 12–15 degrees. Advantages include the ability to acquire a volumetric data set that can be sectioned into thinner sections than typically used for 2-D images, generally in the 2.5–3.0 mm per slice range, with contiguous slices, and with images that can be post-processed into other imaging planes. Although there are differences between some of the sequence features seen between different MR systems, fat suppression tends to be superior with greater uniformity, as compared to 2D SGE. On some MR systems, it is also possible to image a larger volume of tissue during the same breath-hold period, than with 2D-SGE. A potential limitation of 3D SGE imaging has been diminished contrast to noise. This has led to concern regarding use of this technique, other than for gadolinium enhanced fat-suppressed interstitial phase imaging, where the gadolinium effectively improves the contrast to noise ratio.
Motion-insensitive Spoiled Gradient-echo. One limitation of SGE images, both 2- and 3-D, is relative motion sensitivity and requirement for cooperation by the patient in following breathing instructions. In uncooperative patients, SGE may be modified as a single-shot technique using the minimum TR to achieve breathing-independent images. Such sequences have included so-called magnetization prepared rapid acquisition gradient echo (MP-RAGE), and turbo-fast low angle shot (Turbo FLASH).[9] This technique has been achieved using magnetization-prepared SGE, where an inversion prepulse leads to the ability to improve T1-weighted contrast during a short acquisition single slice acquisition. As the protons recover magnetization, a single slice short TR SGE imaging sequence is performed. An inversion time of around 0.5 s provides optimal T1-weighted contrast, and sufficient time to allow the protons to recover between slices leads to an effective slice-to-slice TR of no less than 1.5 s. This technique can be performed to yield through-plane flowing blood either bright or dark, by making the prepulse either slice-selective or non-selective, respectively. Limitations of this technique have included the inability to obtain as high or predictable T1-weighted contrast as with standard SGE (Fig. 5). Another limitation is that the magnetization prepared gradient echoes slice-by-slice technique cannot be used for dynamic gadolinium enhanced imaging of the liver, particularly during the hepatic arterial dominant phase. As each slice requires between around 1.5 s to acquire, the time difference accumulated between the top and bottom liver slices is too great to capture the entire liver in the arterial phase of enhancement. In contrast, the standard SGE sequences, although motion sensitive, offer much superior time resolution for the entire volume of tissue imaged, with the critical contrast data acquired in less than 5 s, and with this data time-averaged throughout the entire set of slices, facilitating capture of the entire liver in the same phase of contrast enhancement.
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Figure 5. (click image to zoom) T1-weighted magnetization prepared gradient echo (GE) sequence (turbo-fast low angle shot [Turbo FLASH]) demonstrates the normal liver without motion artifacts in (a) non-contrast; (b) arterial phase; and (c) late phase images. |
The predominant information provided by T2-weighted sequences are: (i) the presence of increased fluid in diseased tissue, which results in high signal intensity; (ii) the presence of chronic fibrotic tissue, which results in low signal intensity; and (iii) the presence of iron deposition, which results in very low signal intensity.
Echo-train Spin-echo Sequences. The principle of echo-train spin-echo sequences is to summate multiple echoes within the same repetition time interval to decrease examination time, increase spatial resolution, or both. We routinely employ single shot techniques for liver imaging termed HASTE (half fourier acquisition single shot turbo spin echo) or single shot fast spin-echo.[2,3] This is a slice-by-slice technique, where a single slice-selective excitation pulse is followed by a series of echoes, typically using between 80 and 180 pulses, each separated by around 3 ms, to fill in k-space for the entire slice.[3] The T2-weighted contrast is achieved by using the echoes obtained around 80–90 ms for filling central k-space, where central k-space is responsible for image contrast. Although the theoretical TR is infinite, each slice requires around 1.2–1.5 s before continuing to the next slice. However, the motion sensitive component represents only a smaller fraction of the entire acquisition period, making this technique relatively insensitive to breathing artifacts. Echo-train spin-echo has achieved widespread use because of these advantages. In contrast, conventional T2 spin-echo sequences are lengthy and suffer from patient motion and increased examination time.[10] The major disadvantage of echo-train sequences is that T2 differences between tissues are decreased. In the liver, the T2 difference between diseased and background normal liver may be small, and the T2-averaging effects of summated multiple echoes blur this T2 difference (Fig. 6). This results in relatively diminished lesion conspicuity for lesions with mildly elevated T2-weighted signal intensity, such as hepatocellular carcinoma, as compared to standard spin echo sequences. Fortunately, diseases with T2 values similar to those of liver generally have longer T1 values than liver, so that lesions poorly visualized on echo-train spin-echo are generally well visualized on SGE or immediate postgadolinium SGE images as low-signal lesions.
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Figure 6. (click image to zoom) T2-weighted breathing independent single shot-echo-train spin-echo (SS-ETSE) sequence (a) in coronal plane, and breath hold fat suppressed SS-ETSE sequence (b) reveal a metastasis in the left liver lobe (arrows). |
Echo-train spin-echo, and T2-weighted sequences in general, are important for evaluating the liver. In liver masses, T2-weighted images predominantly are important for lesion characterization, while T1-weighted images are important for both lesion detection sensitivity and characterization. T2-weighted images also are important for assessment of diffuse liver disease, including iron deposition, edema related to active liver disease, and fibrosis. Echo-train T2-weighted sequences are important for assessment of fluid filled structures, including bile duct, gall bladder, pancreatic duct, stomach and bowel, as well as cysts or cystic masses, abscesses or collections, or free fluid in the abdomen or pelvis. The relative resistance of echo-train images to motion degradation generally yields better resolution of structures internal to cystic masses, such as the septations within a pancreatic serous or mucinous tumor. MR cholangiopancreatography (MRCP) is based on modified echo-train sequences, where the effective TE is made longer, in the order of 250–500 ms. Lengthening the TE results in heavily T2-weighted high contrast images that yield most soft tissues dark, and makes fluid in bile ducts, gall bladder and pancreatic duct very bright. MRCP can be performed in thin sections of 3–4 mm for higher resolution, or by using a single thick slab of 3–4 cm, to include the majority of the pancreatic and bile duct in a single image. Echo-train imaging is well suited to bowel due to insensitivity to both respiratory motion and bowel peristalsis, and relative resistance to distorting paramagnetic effects of intraluminal bowel gas as a result of repeated refocusing echo pulses.
Fat is high in signal intensity on echo-train spin-echo sequences in comparison to conventional spin-echo sequences, in which fat is intermediate in signal intensity. Fat may also be problematic in the liver because fatty liver will be high in signal intensity on echo-train spin-echo sequences, thereby diminishing contrast with the majority of liver lesions, which are generally high in signal intensity on T2-weighted images. It may be essential to use fat suppression on T2-weighted echo-train spin-echo sequences for liver imaging. Fat suppression should generally be applied for at least one set of images of the liver to ensure optimal contrast between high signal abnormalities, such as fluid collections or cystic masses, and adjacent intra-abdominal fat.
MRI is currently considered an expensive and time intensive imaging modality, which has hampered its appropriate utilization. Decreasing study time and the number of sequences used can dramatically reduce the operational expense of MRI studies.[2] This may be performed most reasonably in the setting of follow-up examinations. Depending on the amount of information needed, a follow-up study that employs coronal single-shot echo-train spin echo, transverse precontrast SGE, arterial and venous phase postgadolinium SGE, and 2-min interstitial phase postgadolinium fat-suppressed SGE provides relatively comprehensive information in a 15 min study time.[5] An even more curtailed examination can be performed if only change in lesion size is being assessed. An adrenal mass or lymphadenopathy may be adequately followed by precontrast SGE alone and, in the case of an adrenal adenoma, using dual echo out-of-phase and in-phase SGE.
Uncooperative Patients. It is crucial to recognize that separate protocols are required for uncooperative patients. In general, uncooperative patients fall into two categories: (i) those who cannot suspend respiration but breathe in a regular fashion; and (ii) those who cannot suspend respiration and cannot breathe in a regular fashion. The most common patient population that fits into the first group are sedated pediatric patients. Agitated patients are the most commonly encountered population who fit into the second group. Imaging strategies differ for each.
In sedated patients, substitution of breath-hold images (e.g. SGE) can be made readily with breathing-averaged spin echo images, the image quality of which is improved by using fat suppression. With sedation, breathing is in a more regular pattern than that observed for all other patients. Additionally, breathing-independent T2-weighted single-shot echo-train spin-echo is useful, as is T1-weighted MP-RAGE, if dynamic gadolinium-enhanced images are required.
In patients who are agitated, only single-shot techniques should be used, including breathing-independent T2-weighted single-shot echo train spin echo and T1-weighted MP-RAGE pre- and postgadolinium administration.
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http://www.medscape.com/viewarticle/530267_2 | |||
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