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(Radiographics. 1999;19:373-382.)
© RSNA, 1999


SCIENTIFIC EXHIBIT

Fat Suppression in MR Imaging: Techniques and Pitfalls

Emmanuelle M. Delfaut, MD1, Javier Beltran, MD3, Glyn Johnson, PhD4, Jean Rousseau, PhD2, Xavier Marchandise, MD, PhD2 and Anne Cotten, MD1

1 Departments of Radiology (E.M.D., A.C.)
2 Nuclear Medicine (J.R., X.M.), Hospital Roger Salengro, Boulevard du Professeur J. Leclercq, 59037 Lille, France
3 Department of Radiology, Hospital for Joint Diseases, New York, NY (J.B.)
4 Department of Radiology, New York University Medical Center, New York, NY (G.J.)


    Abstract
 Top
 Abstract
 INTRODUCTION
 FAT SATURATION
 INVERSION-RECOVERY IMAGING
 OPPOSED-PHASE IMAGING
 OTHER METHODS
 SUMMARY
 References
 
Fat suppression is commonly used in magnetic resonance (MR) imaging to suppress the signal from adipose tissue or detect adipose tissue. Fat suppression can be achieved with three methods: fat saturation, inversion-recovery imaging, and opposed-phase imaging. Selection of a fat suppression technique should depend on the purpose of the fat suppression (contrast enhancement vs tissue characterization) and the amount of fat in the tissue being studied. Fat saturation is recommended for suppression of signal from large amounts of fat and reliable acquisition of contrast material–enhanced images. The main drawbacks of this technique are sensitivity to magnetic field nonuniformity, misregistration artifacts, and unreliability when used with low-field-strength magnets. Inversion-recovery imaging allows homogeneous and global fat suppression and can be used with low-field-strength magnets. However, this technique is not specific for fat, and the signal intensity of tissue with a long T1 and tissue with a short T1 may be ambiguous. Opposed-phase imaging is a fast and readily available technique. This method is recommended for demonstration of lesions that contain small amounts of fat. The main drawback of opposed-phase imaging is unreliability in the detection of small tumors embedded in fatty tissue.

Index Terms: Fat, MR, **.1214152 • Magnetic resonance (MR), fat suppression, **.121415 • Magnetic resonance (MR), inversion recovery, **.121413 • Magnetic resonance (MR), phase imaging, **.121419


    INTRODUCTION
 Top
 Abstract
 INTRODUCTION
 FAT SATURATION
 INVERSION-RECOVERY IMAGING
 OPPOSED-PHASE IMAGING
 OTHER METHODS
 SUMMARY
 References
 
Fat suppression is used in routine magnetic resonance (MR) imaging for many purposes, but two main indications can be identified. First, fat suppression is used to suppress the signal from normal adipose tissue to reduce chemical shift artifact or improve visualization of uptake of contrast material. The second main use is tissue characterization, particularly in adrenal gland tumors, bone marrow infiltration, fatty tumors, and steatosis. It is important to distinguish between these indications because the optimal fat suppression technique depends on the amount of lipid that requires signal suppression. The best techniques for suppressing signal from normal white fat composed of a large proportion of lipid are different from the best techniques for suppressing lipid signal in fatty infiltration or tumors containing a small amount of fat.

White fat is composed of lobules, which are demarcated by septa of loose connective tissue and supported by a stroma; the stroma accounts for approximately 5% of the total mass of the tissue (1). Within adipocytes, lipids are stored in large vacuoles. The normal composition of lipids is 99% triglycerides and less than 1% cholesterol, phospholipids, and free fatty acids (2). During an MR imaging acquisition, two different components produce a signal from white fat: protons from lipids (>80% of the signal) and protons from hydrogen atoms in water located within loose connective tissue (<20% of the signal) (3).

Fat suppression is a generic term that includes various techniques, each with specific advantages, disadvantages, and pitfalls. Lipid protons and hydrogen protons from water behave differently during an MR imaging acquisition, and fat suppression techniques are based on these differences. Two major properties are involved: First, there is a small difference in resonance frequency, {delta}f0, between lipid and water protons, which is related to the different electronic environments. This so-called chemical shift allows frequency-selective fat saturation. Second, the difference in T1 between adipose tissue and water can be used to suppress the fat signal with inversion-recovery techniques. The chemical shift between lipid and water also allows fat suppression with opposed-phase imaging.


    FAT SATURATION
 Top
 Abstract
 INTRODUCTION
 FAT SATURATION
 INVERSION-RECOVERY IMAGING
 OPPOSED-PHASE IMAGING
 OTHER METHODS
 SUMMARY
 References
 
During a fat saturation acquisition, a frequency-selective saturation radio-frequency pulse with the same resonance frequency as that of lipids is applied to each slice-selection radio-frequency pulse. A homogeneity spoiling gradient pulse is applied immediately after the saturation pulse to dephase the lipid signal. The signal excited by the subsequent slice-selection pulse contains no contribution from lipid (Fig 1) (4).



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Figure 1.  Fat saturation. Diagram shows a frequency-selective saturation radio-frequency pulse applied to each slice-selection radio-frequency pulse. OL = olefinic fatty acid.

 
Advantages
Fat saturation is lipid specific; therefore, this method is reliable for contrast material–enhanced T1-weighted imaging and tissue characterization particularly in areas with a large amount of fat. Fat saturation is also useful for avoiding chemical shift misregistration artifacts. Because fat suppression is achieved by preceding the normal acquisition with a frequency-selective saturation pulse, fat saturation can be used with any imaging sequence. Signal in nonadipose tissue is practically unaffected as long as the saturation pulse frequency and bandwidth are properly selected; the signal-to-noise ratio in adipose tissue is of course decreased. Fat saturation thus allows good visualization of small anatomic details and is very useful, for example, in postcontrast MR arthrography (Fig 2).



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Figure 2.  MR arthrography of the knee. Coronal fat saturation T1-weighted MR image (960/20 [repetition time msec/echo time msec]) shows contrast material within a small radial tear of the medial meniscus (arrow).

 
Disadvantages
To achieve reliable fat saturation, the frequency of the frequency-selective saturation pulse must equal the resonance frequency of lipid. However, inhomogeneities of the static magnetic field will shift the resonance frequencies of both water and lipid. In these areas, the saturation pulse frequency might not equal the lipid resonance frequency; this discrepancy would result in poor fat suppression. Even worse, the saturation pulse can saturate the water signal instead of the lipid signal; the result would be a water-suppressed image. Static field inhomogeneities inherent in magnet design are relatively small in modern magnets and can be reduced by decreasing the field of view, centering over the region of interest, and autoshimming. However, substantial inhomogeneities can be caused by local magnetic susceptibility differences such as those found at air-bone interfaces in the lower portion of the orbit (Fig 3) (5) and in the nasopharynx, at air-fat-liver interfaces in the right anterior diaphragmatic region (6), or around foreign bodies like metal or air collections. Inhomogeneities are also likely to occur in areas of sharp variations in anatomic structures (Fig 4) (7).



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Figure 3.  Failure of fat saturation. Enhanced coronal fat saturation T1-weighted spin-echo MR image (810/14) of the head shows high signal intensity within the rectus inferior bulbi muscle (arrows). This high signal intensity is related to failure of fat suppression. (Courtesy of Bruno Pertuson, MD, Hospital Roger Salengro, Lille, France.)

 


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Figure 4.  Incomplete fat saturation. Coronal fat saturation T2-weighted fast spin-echo MR image (4,700/112) of the head and neck obtained with a large field of view (300 x 300 mm) shows areas of marked spatial variation. Fat suppression is incomplete within subcutaneous fat and deep spaces of the neck.

 
Inhomogeneities in the radio-frequency field can also reduce the efficacy of fat saturation. For complete saturation of the lipid signal, the saturation pulse must be exactly 90°. Where the radio-frequency field is inhomogeneous, the pulse will be greater or less than 90° and will leave residual fat signal. The problem can be exacerbated by use of surface coils. Even when surface coils are used for reception only, the presence of such coils can distort the transmitter field sufficiently so that substantial fat signal is left.

Besides technical problems, there are two other reasons why fat saturation can result in incomplete fat suppression. First, the fraction of adipose tissue that is water will not be saturated. Second, a small fraction of fatty acids (5%) have the same resonance frequency as water (3), and signal from these fatty acids will be unsuppressed; such fatty acids, which are free or bound to triglycerides, are called olefinic fatty acids or alkenes. Therefore, detection of a small amount of fat can be impaired.

The chemical shift between lipid and water increases with the strength of the magnetic field (at 1.0 T, {delta}f0 {approx} 150 Hz; at 1.5 T, {delta}f0 {approx} 220 Hz). Fat suppression is therefore of lower quality when low-field-strength magnets are used because {delta}f0 is small. It is thus difficult to achieve effective lipid saturation without also producing water saturation.

Finally, because the time required for application of the saturation pulse is about 10 msec, fat saturation can substantially increase the imaging time. In T2-weighted imaging, the additional time is small compared with the acquisition time (ie, the time between the initial excitation pulse and the end of the read period). However, in fast gradient-echo imaging, the saturation time and acquisition time are comparable, a fact that leads to large increases in the imaging time.


    INVERSION-RECOVERY IMAGING
 Top
 Abstract
 INTRODUCTION
 FAT SATURATION
 INVERSION-RECOVERY IMAGING
 OPPOSED-PHASE IMAGING
 OTHER METHODS
 SUMMARY
 References
 
In inversion-recovery imaging, suppression of the fat signal is based on differences in the T1 of the tissues (810). The T1 of adipose tissue is shorter than the T1 of water. After a 180° inversion pulse, the longitudinal magnetization of adipose tissue will recover faster than that of water. If a 90° pulse is applied at the null point of adipose tissue, adipose tissue will produce no signal whereas water will still produce a signal (Fig 5). Therefore, the fat signal can be suppressed by using a short TI inversion-recovery (STIR) sequence. As long as the repetition time is much longer than the T1, the null point will be at a TI (TInull) equal to 0.69 times the T1 (10,11). The T1 and hence the optimal TInull for achieving suppression of adipose tissue signal depend on the magnetic field strength. At 1.5 T, TInull occurs at approximately 130–170 msec.



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Figure 5.  Inversion-recovery imaging. Diagram shows the behavior of adipose tissue signal and water signal during an inversion-recovery sequence. Note that the water signal has not fully recovered at the beginning of the imaging sequence. FSE = fast spin-echo imaging, LM = longitudinal magnetization, SE = spin-echo imaging, TI = inversion time.

 
STIR imaging is usually performed with a fast spin-echo readout sequence, which allows shorter acquisition times than does a conventional spin-echo sequence.

Advantages
The STIR method suppresses the signal of whole adipose tissue including the water fraction. This is the only method that is insensitive to magnetic field inhomogeneities and can be used with low-field-strength magnets. In addition, T2 and T1 differences contribute additively to the contrast in STIR sequences. Therefore, the contrast is extremely good and tissues with long T1 and long T2 appear very bright (8). This property can enhance tumor detection.

Disadvantages
As the imaging sequence begins at TInull, most of the protons have not completed relaxation and are therefore still partially saturated. This situation will produce overall signal loss (Fig 5), and in general inversion-recovery images have low signal-to-noise ratios.

Signal intensity in inversion-recovery sequences is related to the absolute value of the longitudinal magnetization (ie, regardless of whether it has passed the null point). Therefore, tissue with a short T1 and tissue with a long T1 may produce the same signal intensity (Fig 6). However, the most misleading disadvantage is that the fat suppression is nonspecific (12). Signal from tissue or fluid with a T1 similar to that of fat will also be suppressed. Examples of such tissue or fluid are mucoid tissue, hemorrhage (Fig 7), proteinaceous fluid, and gadolinium (Fig 8) or melanin in a given concentration. Conversely, areas of fatty infiltration or tumors containing fat might not have the same T1 as white fat. Therefore, the TInull used to perform STIR imaging might not fully suppress the signal from these areas or tumors. Fat composition and therefore the optimal TI can also vary with anatomic location and between individuals. To determine the optimal TI for suppression of the signal from normal white fat, TI tuning techniques based on the spectral display have been developed (13,14). However, these techniques optimize lipid suppression only and include signal from the water fraction of adipose tissue (15).



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Figure 6.  Ambiguous signal intensity with inversion-recovery imaging. Diagram shows how tissue with a short T1 and tissue with a long T1 may produce the same signal intensity. LM = longitudinal magnetization.

 


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Figure 7a.  Incidentally discovered renal mass in a patient referred for evaluation of liver metastases. At surgery, a renal cell carcinoma surrounded by a large area of hemorrhage was found. (a) Axial fat saturation T1-weighted gradient-echo MR image (183/4.5, 80° flip angle) shows a heterogeneous mass related to the left kidney with areas of intermediate and high signal intensity (arrow). The hyperintense areas are most likely related to hemorrhage. (b) Corresponding opposed-phase MR image (146/2.5, 90° flip angle) shows the same findings (arrow). (c) Corresponding inversion-recovery MR image (4,200/76, 160-msec TI) shows suppression of signal from some of the hyperintense areas (arrow). (Figs 7a7c courtesy of Glenn A. Krinsky, MD, New York University, New York, NY.)

 


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Figure 7b.  Incidentally discovered renal mass in a patient referred for evaluation of liver metastases. At surgery, a renal cell carcinoma surrounded by a large area of hemorrhage was found. (a) Axial fat saturation T1-weighted gradient-echo MR image (183/4.5, 80° flip angle) shows a heterogeneous mass related to the left kidney with areas of intermediate and high signal intensity (arrow). The hyperintense areas are most likely related to hemorrhage. (b) Corresponding opposed-phase MR image (146/2.5, 90° flip angle) shows the same findings (arrow). (c) Corresponding inversion-recovery MR image (4,200/76, 160-msec TI) shows suppression of signal from some of the hyperintense areas (arrow). (Figs 7a7c courtesy of Glenn A. Krinsky, MD, New York University, New York, NY.)

 


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Figure 7c.  Incidentally discovered renal mass in a patient referred for evaluation of liver metastases. At surgery, a renal cell carcinoma surrounded by a large area of hemorrhage was found. (a) Axial fat saturation T1-weighted gradient-echo MR image (183/4.5, 80° flip angle) shows a heterogeneous mass related to the left kidney with areas of intermediate and high signal intensity (arrow). The hyperintense areas are most likely related to hemorrhage. (b) Corresponding opposed-phase MR image (146/2.5, 90° flip angle) shows the same findings (arrow). (c) Corresponding inversion-recovery MR image (4,200/76, 160-msec TI) shows suppression of signal from some of the hyperintense areas (arrow). (Figs 7a7c courtesy of Glenn A. Krinsky, MD, New York University, New York, NY.)

 


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Figure 8a.  Signal suppression with inversion-recovery imaging. Different dilutions of gadopentetate dimeglumine (Magnevist; Berlex Laboratories, Wayne, NJ) in 0.9% saline solution were used to produce solutions with a concentration of 2.0 x 10-3, 1.0 x 10-3, 5.0 x 10-4, and 2.5 x 10-4 mmol/mL (shown from left to right). (a) T1-weighted spin-echo MR image (460/20) shows high signal intensity within each tube. The high signal intensity increases progressively with gadolinium concentration. (b) Corresponding inversion-recovery MR image (4,100/60, 165-msec TI) shows suppression of signal from the 5.0 x 10-4 mmol/mL solution. (Figs 8a and 8b reprinted, with permission, from reference 12.)

 


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Figure 8b.  Signal suppression with inversion-recovery imaging. Different dilutions of gadopentetate dimeglumine (Magnevist; Berlex Laboratories, Wayne, NJ) in 0.9% saline solution were used to produce solutions with a concentration of 2.0 x 10-3, 1.0 x 10-3, 5.0 x 10-4, and 2.5 x 10-4 mmol/mL (shown from left to right). (a) T1-weighted spin-echo MR image (460/20) shows high signal intensity within each tube. The high signal intensity increases progressively with gadolinium concentration. (b) Corresponding inversion-recovery MR image (4,100/60, 165-msec TI) shows suppression of signal from the 5.0 x 10-4 mmol/mL solution. (Figs 8a and 8b reprinted, with permission, from reference 12.)

 

    OPPOSED-PHASE IMAGING
 Top
 Abstract
 INTRODUCTION
 FAT SATURATION
 INVERSION-RECOVERY IMAGING
 OPPOSED-PHASE IMAGING
 OTHER METHODS
 SUMMARY
 References
 
The opposed-phase technique is based on phase differences in images acquired at different echo times (1620). Phase is the angle of the magnetization vector in the transverse plane. Because lipid protons and water protons have different resonance frequencies, the phases of these protons relative to each other change with time after the initial excitation (Fig 9). Immediately after excitation, the lipid signal and water signal are in phase (ie, the phase difference between them is zero). However, water protons precess fractionally faster than lipid protons; therefore, after a few milliseconds, the phase difference between the two is 180° (ie, the phase is opposed). After a few more milliseconds, the water spins complete a 360° rotation relative to the lipid spins and the spins are again in phase. The spins can thus be sampled in an in-phase or opposed-phase condition by selecting the appropriate echo time. In general, this technique is applicable only to gradient-echo sequences. The 180° refocusing pulse used in spin-echo sequences always brings the lipid signal and water signal back into phase regardless of the echo time.



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Figure 9.  Opposed-phase and in-phase imaging. Diagram shows the behavior of lipid (L) signal and water (W) signal relative to the echo time (TE) during a gradient-echo (GRE) sequence (1.5 T). OL = olefinic fatty acid, t = time.

 
During an MR imaging sequence, the signal within a voxel is the vector sum of the lipid and water signals of the protons within that voxel (Fig 10). The lipid signal and water signal are additive in in-phase images, but in opposed-phase images the signal is the difference between the lipid and water signals. Therefore, opposed-phase imaging reduces the signal from fatty tissue.



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Figure 10.  Opposed-phase imaging. Diagram shows the signal within a heterogeneous voxel. The signal is the vector sum of the lipid (L) and water (W) signals. According to the phase of these signals, they add or subtract and produce a higher or lower signal within the voxel. OL = olefinic fatty acid.

 
Opposed-phase imaging is best suited to suppressing the signal from tissues that contain similar amounts of lipid and water. In tissues that contain predominantly lipid or predominantly water, the reduction in signal is small. For example, in adipose tissue, voxels contain mainly adipocytes and the signal from water is much smaller than the signal from lipid. The small amount of water produces only a small reduction in signal. Therefore, the adipose tissue signal is fairly high (Fig 11) and the opposed-phase image is poorly fat suppressed. Conversely, voxels that contain tissue infiltrated by fat or only small areas of adipose tissue have a low signal in opposed-phase images. In this situation, the lipid and water signals partially cancel. The signal in opposed-phase imaging is lower than the signal produced with fat saturation: In opposed-phase imaging, the signal consists of the water signal minus the lipid signal; with fat saturation, the signal consists of the water signal alone (Fig 12). For this reason, opposed-phase images are useful for detection of small amounts of fat, for example, in adrenal gland tumor (Fig 13) (17,19) or steatosis (19). At borders between fat and nonfatty tissue, signal from adjacent lipids and water can be equal; this situation results in a characteristic signal void termed the india ink artifact (Fig 13) (19). The recognizable look of opposed-phase images is due to this feature.



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Figure 11.  Opposed-phase imaging versus fat saturation. Diagram shows the respective signals from tissue with a large amount of fat. L = lipid, OL = olefinic fatty acid, W = water.

 


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Figure 12.  Opposed-phase imaging versus fat saturation. Diagram shows the respective signals from tissue with a small amount of fat. L = lipid, OL = olefinic fatty acid, W = water.

 


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Figure 13a.  Adrenal gland tumor. (a) Axial in-phase gradient-echo MR image (163/4, 90° flip angle) of the abdomen shows a small, solid adrenal mass (arrow) surrounded by a faint halo of high signal intensity. (b) Corresponding opposed-phase MR image (163/2.5, 90° flip angle) shows the halo as hypointense because of equal amounts of lipid and water in this area. Note the india ink artifact (arrowheads) around structures surrounded by fat. In these areas, the amounts of lipid and water are also equal. However, the fat signal is not fully suppressed in adipose tissue (*), where the amount of lipid is much larger than the amount of water. (Figs 13a and 13b courtesy of Glenn A. Krinsky, MD, New York University, New York, NY.)

 


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Figure 13b.  Adrenal gland tumor. (a) Axial in-phase gradient-echo MR image (163/4, 90° flip angle) of the abdomen shows a small, solid adrenal mass (arrow) surrounded by a faint halo of high signal intensity. (b) Corresponding opposed-phase MR image (163/2.5, 90° flip angle) shows the halo as hypointense because of equal amounts of lipid and water in this area. Note the india ink artifact (arrowheads) around structures surrounded by fat. In these areas, the amounts of lipid and water are also equal. However, the fat signal is not fully suppressed in adipose tissue (*), where the amount of lipid is much larger than the amount of water. (Figs 13a and 13b courtesy of Glenn A. Krinsky, MD, New York University, New York, NY.)

 
Because resonance frequency and magnetic field strength are related, the echo time required to obtain in-phase or opposed-phase images depends on the magnetic field strength.

Advantages
The opposed-phase technique is simple, fast, and available on every MR imaging system. The ability to demonstrate small amounts of fat and fat-water mixtures is the strongest advantage of this technique (1720). In addition, opposed-phase imaging is independent of static field inhomogeneity because the method depends on the relative precession frequencies of lipid and water spins and not on the absolute values of these frequencies.

Disadvantages
As discussed earlier, opposed-phase imaging does not suppress the signal from adipose tissue. In addition, it can be difficult to detect small tumors embedded in fat (21) (Fig 11) because the signal from the tumor can be nulled by the signal from surrounding adipose tissue. Furthermore, after injection of contrast material, contrast material uptake can be undetectable or result in paradoxical increased fat suppression (22). This pitfall can occur in imaging of the breast, where tumors are embedded in large amounts of adipose tissue.


    OTHER METHODS
 Top
 Abstract
 INTRODUCTION
 FAT SATURATION
 INVERSION-RECOVERY IMAGING
 OPPOSED-PHASE IMAGING
 OTHER METHODS
 SUMMARY
 References
 
Like the opposed-phase technique, the technique described by Dixon (23) is based on phase differences. With the Dixon method, both in-phase and opposed-phase images are acquired. (Dixon [23] acquired the images with a spin-echo sequence in which the sampling period was offset slightly from the spin-echo center.) The sum of these images produces a pure water image; the difference between these images produces a pure lipid image. The Dixon method requires a minimum of two data acquisitions and is as susceptible to static field inhomogeneities as is fat saturation. Therefore, the Dixon method is rarely used nowadays. Similar techniques that are faster or that correct for static field inhomogeneity have been developed (2426). However, these techniques are not currently implemented on most MR imaging systems.

In the water excitation technique (27,28), combinations of radio-frequency pulses are used to excite only water; lipid spins are left in equilibrium and thus produce no signal. Like fat saturation, water excitation is susceptible to static field inhomogeneities. However, water excitation adds only 1–2 msec to the repetition time, whereas fat saturation adds approximately 10 msec. Therefore, water excitation has a time advantage in fast gradient-echo imaging. However, water excitation is a relatively new technique and is currently used in few clinical studies.


    SUMMARY
 Top
 Abstract
 INTRODUCTION
 FAT SATURATION
 INVERSION-RECOVERY IMAGING
 OPPOSED-PHASE IMAGING
 OTHER METHODS
 SUMMARY
 References
 
Fat saturation is recommended for suppression of signal from large amounts of fat and reliable acquisition of contrast-enhanced images. The main drawbacks of this technique are sensitivity to magnetic field nonuniformity, misregistration artifacts, and unreliability when used with low-field-strength magnets. Inversion-recovery imaging allows homogeneous and global fat suppression and can be used with low-field-strength magnets. However, this technique is not specific for fat, and the signal intensity of tissue with a long T1 and tissue with a short T1 may be ambiguous. Opposed-phase imaging is a fast and readily available technique. This method is recommended for demonstration of lesions that contain small amounts of fat. The main drawback of opposed-phase imaging is unreliability in the detection of small tumors embedded in fatty tissue.


    Footnotes
 
Address reprint requests to E.M.D.

**. Multiple body systems Back

Presented as a scientific exhibit at the 1997 RSNA scientific assembly.

Abbreviations: STIR = short inversion time inversion recovery TI = inversion time

Received for publication April 1, 1998. Revision received May 1, 1998. July 6, 1998. Accepted for publication July 9, 1998.


    References
 Top
 Abstract
 INTRODUCTION
 FAT SATURATION
 INVERSION-RECOVERY IMAGING
 OPPOSED-PHASE IMAGING
 OTHER METHODS
 SUMMARY
 References
 

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