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DOI:10.2214/AJR.05.0695
AJR 2006; 187:W103-W106
© American Roentgen Ray Society

Technical Innovation

Opposed-Phase MRI for Fat Quantification in Fat-Water Phantoms with 1H MR Spectroscopy to Resolve Ambiguity of Fat or Water Dominance

Jerry S. Chang1, Bachir Taouli2, Nouha Salibi3, Elizabeth M. Hecht2, Deanna G. Chin4 and Vivian S. Lee2

1 Westwood Radiology Associates, Pascack Valley Hospital, Westwood, NY 07675.
2 Department of Radiology, NYU Medical Center, 560 First Ave., TCH-HW 202, New York, NY 10016.
3 Siemens Medical Solutions, Malvern, PA 19355.
4 Department of Radiology, Robert Wood Johnson University Hospital, East Brunswick, NJ 08816.

Received April 23, 2005; accepted after revision August 22, 2005.

 
Jerry S. Chang and Bachir Taouli contributed equally to this article.

Address correspondence to B. Taouli (bachir.taouli{at}med.nyu.edu).

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Abstract
Top
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 References
 
OBJECTIVE. The purpose of the study was to quantify the fat fraction in nine fat-water phantoms containing 0-80% fat using opposed-phase imaging with the qualitative guidance of 1H MR spectroscopy (MRS), which was used by observer 1 to visually assess the sizes of the water and fat peaks to apply two alternative mathematic formulas for the calculation of the fat fraction. In addition, the fat fraction was also quantified directly with 1H MRS as an independent method by two observers (observers 2 and 3).

CONCLUSION. The fat fraction calculated with opposed-phase imaging (FFOPI) and that calculated with 1H MRS (FFMRS) correlated well with the known fat fractions of the phantoms (FFP): r = 0.99 for FFOPI; p < 0.0001 and r = 0.96-0.98 for FFMRS; p < 0.001, for observers 2 and 3, respectively. Opposed-phase imaging should be combined with 1H MRS to ensure accurate quantification of the fat fraction.

Keywords: liver disease • MRI • SPECT


Introduction
Top
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 References
 
The opposed-phase MRI technique is based on phase differences in images acquired using different TEs. Fat and water signals are additive on in-phase images and subtracted on opposed-phase images. Therefore, opposed-phase imaging reduces the signal from tissues containing intravoxel fat. Opposed-phase imaging is commonly used to identify tissues containing a significant proportion of intracellular microscopic triglycerides, such as fatty liver [1-5]. However, quantification of the hepatic fat fraction might be limited with opposed-phase imaging because of the ambiguity of fat or water dominance—that is, a high fat fraction will result in a similar signal intensity (SI) change on opposed-phase imaging as will a low fat fraction. A high or low percentage of fat determines a signal drop on opposed-phase MRI that looks similar at qualitative visual analysis. Consequently, to date, opposed-phase imaging has proven inaccurate for quantification of high fat fraction in the liver [1, 5]. To help resolve fat-water ambiguity, qualitative assessment of a quick 1H MR spectroscopic (MRS) acquisition can be performed. To the best of our knowledge, there is no study that has combined the use of opposed-phase imaging with qualitative 1H MRS to quantify the fraction of fat in the liver.

The purpose of our investigation was to correlate the fraction of fat in fat-water phantoms measured on opposed-phase imaging (FFOPI) and to use 1H MRS to resolve the ambiguity of fat or water dominance.


Materials and Methods
Top
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 References
 
Phantom Composition
Nine phantoms with various fractions of fat were produced by homogenizing a mixture of commercially available vegetable canola oil and fresh calf liver. Liver and oil were mixed using a blender, and a homogeneous mayonnaise-like emulsion was subsequently obtained. The mixture was put in a plastic container measuring 6 x 8 cm.

The phantoms contained 0%, 10%, 20%, 30%, 40%, 50%, 60%, 70%, and 80% fat by weight (using a commercially available scale). Each phantom was placed in a water bath to augment magnetic field homogeneity. The water bath served as an SI calibrator for opposed-phase images.

MRI
The following sequences were performed using a 1.5-T magnet (Magnetom Quantum Symphony, Siemens Medical Solutions) and a body coil.

Opposed-phase imaging—A dual-echo opposed-phase gradient-recalled echo T1-weighted sequence was performed in the coronal plane using the following parameters: TR, 167 msec; TE, 4.76 (in-phase) and 2.38 (opposed-phase) msec; flip angle, 80°; matrix, 95 x 256; field of view, 150 x 300 mm; 1 signal averaged; 4 slices of 8-mm thickness and 2-mm gap; and acquisition time, 14 seconds.


Figure 1
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  		Fig. 1A —In-phase and opposed-phase imaging of fat-water phantoms. Curve of signal intensity (SI) of fat-water phantoms on in-phase (•) and opposed-phase ({blacksquare}) images versus phantom fat fraction (FFP). Arrow points to maximum SI loss on opposed-phased images for fat fraction of 50%.

 


Figure 2
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  		Fig. 1B —In-phase and opposed-phase imaging of fat-water phantoms. Corresponding in-phase and opposed-phase images and 1H MR spectroscopy (MRS) images of three fat-water phantoms placed in water bath; phantoms are composed of 30% (B), 50% (C), or 70% (D) fat. Water peak (short arrow) is 4.7 ppm and fat peak (long arrow) ranges from 1 to 1.5 ppm on MRS images. Example of placement of regions of interest (circles, C) is shown in C. Maximum signal loss on opposed-phase images is seen for phantom with 50% fat (C). Phantoms with 30% (A) and 70% (B) fat are indistinguishable on opposed-phase images. Without MRS to resolve for fat-water dominance, high fat fraction may be misinterpreted as low fat fraction.

 


Figure 3
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  		Fig. 1C —In-phase and opposed-phase imaging of fat-water phantoms. Corresponding in-phase and opposed-phase images and 1H MR spectroscopy (MRS) images of three fat-water phantoms placed in water bath; phantoms are composed of 30% (B), 50% (C), or 70% (D) fat. Water peak (short arrow) is 4.7 ppm and fat peak (long arrow) ranges from 1 to 1.5 ppm on MRS images. Example of placement of regions of interest (circles, C) is shown in C. Maximum signal loss on opposed-phase images is seen for phantom with 50% fat (C). Phantoms with 30% (A) and 70% (B) fat are indistinguishable on opposed-phase images. Without MRS to resolve for fat-water dominance, high fat fraction may be misinterpreted as low fat fraction.

 


Figure 4
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  		Fig. 1D —In-phase and opposed-phase imaging of fat-water phantoms. Corresponding in-phase and opposed-phase images and 1H MR spectroscopy (MRS) images of three fat-water phantoms placed in water bath; phantoms are composed of 30% (B), 50% (C), or 70% (D) fat. Water peak (short arrow) is 4.7 ppm and fat peak (long arrow) ranges from 1 to 1.5 ppm on MRS images. Example of placement of regions of interest (circles, C) is shown in C. Maximum signal loss on opposed-phase images is seen for phantom with 50% fat (C). Phantoms with 30% (A) and 70% (B) fat are indistinguishable on opposed-phase images. Without MRS to resolve for fat-water dominance, high fat fraction may be misinterpreted as low fat fraction.

 
1H MRS—A single-voxel 1H MRS sequence (point-resolved spectroscopy [PRESS]) was performed after the opposed-phase imaging sequence using the following parameters: TR/TE, 2,000/30; voxel size, 2.5 x 2.5 x 2.5 cm; 12 signals averaged; acquisition time, 24 seconds; and spectral width, 6.2 ppm.

Image Evaluation
Qualitative evaluation—In- and opposed-phase phantom images were visually inspected for SI changes by a single experienced observer (observer 1) who was a clinical fellow in body MRI at time of the study.

Fat quantification analysis on opposed-phase imaging—With care to avoid bubbles, the same observer (observer 1) used five manually drawn regions of interest (ROIs) randomly selected on each phantom to measure the mean SI on in-phase images (SIIP) and the mean SI on opposed-phase images (SIOP) of the ROIs, with an exact matching location, and measurements were averaged. Random measure was possible after ensuring homogeneous preparation of the phantom using a blender. ROIs included at least 200 pixels. SIIP and SIOP were normalized to the SI of the water bath on in- and opposed-phase images. Opposed-phase images show SI loss because of cancellation of fat and water signals due to differences in precession frequencies so that, theoretically, signal loss on opposed-phase images should be highest for a fat fraction of 50% (Figs. 1A, 1B, 1C, and 1D).


Figure 5
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  		Fig. 2 —Correlation between fat fraction calculated using opposed-phase imaging (FFOPI) with 1H MR spectroscopy for qualitative analysis to resolve ambiguity of fat or water dominance in phantom with known fat fraction (FFP). y = 1.09x - 0.02, R2 = 0.99, p < 0.001.

 
The fat fraction on opposed-phase imaging was calculated as a percentage using the Dixon technique [1] with 1H MRS to resolve the ambiguity of fat or water dominance based on a visual analysis of the size of the fat and water peaks, located at 1.0-1.5 and 4.7 ppm, respectively. If water > fat, FFOPI = (SIIP / SIIP water bath - SIOP / SIOP water bath) / (2 x SIIP / SIIP water bath) x 100. If fat ≥ water, then FFOPI = 1 - (SIIP / SIIP water bath - SIOP / SIOP water bath) / (2 x SIIP / SIIP water bath) x 100.

Fat quantification analysis on MRS—As an independent method, the areas under the water and fat peaks on 1H MRS were analyzed quantitatively by two observers (observers 2 and 3), different from the observer mentioned earlier, who were blinded to the known phantom composition and opposed-phase imaging results. They calculated the fat fraction with 1H MRS using commercially available software (Syngo, Siemens Medical Solutions): FFMRS (%) = [fat peak / (fat peak + water peak)] x 100. The fat peak was measured at 1.0-1.5 ppm, and the water peak was measured at 4.7 ppm. The 1H MRS postprocessing time was less than 1 minute for both qualitative and quantitative use.

Statistical Analysis
Statistical analysis was performed using Minitab software (version 14, Minitab Inc.). The error range and mean absolute error of the fat fractions calculated using opposed-phase imaging and 1H MRS were measured. The FFOPI (for observer 1) and FFMRS (for observers 2 and 3) were correlated with the known phantom fat fraction (FFP) using Spearman's rank correlation coefficient test. A correlation was defined as strong when r > 0.8, moderate for r ranging between 0.6 and 0.8, and weak when r < 0.6. In addition, FFMRS for observers 2 and 3 were correlated using the Spearman's rank correlation coefficient test and by calculating the mean absolute percentage difference between the two observers as FFMRS for observer 2 - FFMRS for observer 3.


Results
Top
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 References
 
Opposed-Phase Imaging
By visual inspection, the phantoms with 30-70% fat (Figs. 1A, 1B, 1C, and 1D) and 40-60% fat were indistinguishable on in- and opposed-phase images. The relationship between SI on in-phase and opposed-phase images and the known phantom fat fraction (FFP) is illustrated on the curve in Figures 1A, 1B, 1C, and 1D, which shows maximum signal loss on opposed-phase images when FFP is 50% and comparable degrees of SI loss in phantoms with small or large amounts of fat.

With the visual analysis of 1H MRS fat-water peak size to guide for fat and water dominance on in-phase and opposed-phase images, there was a strong correlation (r = 0.99, p < 0.0001) between the fat fraction calculated with opposed-phase imaging (FFOPI) and the known fat fraction (FFP) (Fig. 2). The mean absolute error was 3% (range, -3% to 6%). When opposed-phase imaging was used to quantify the fat fraction without 1H MRS, there was a weak correlation between the fat fraction calculated with opposed-phase imaging and the known fat fraction (r = 0.47, p = 0.2).

1H MRS
There was a strong correlation between the fat fraction calculated using 1H MRS (FFMRS) and the known fat fraction (FFP) for both observers (r = 0.96, p < 0.001 for observer 2; and r = 0.98, p < 0.001 for observer 3). FFMRS from observers 2 and 3 were strongly correlated (r = 0.96, p < 0.001). The mean absolute percentage difference for FFMRS measurement between observers was 13% (range, 6-20%), which shows good agreement.


Discussion
Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
References
 
Our in vitro study showed that fat quantification is inaccurate when opposed-phase imaging is used alone—that is, without 1H MRS to resolve the ambiguity of fat or water dominance. Opposed-phase imaging is known to be an accurate method to detect microscopic fat [6]; however, data about the use of opposedphase imaging for liver fat quantification are limited [1-3, 5]. One study combined in vitro and in vivo data [3] and showed a strong correlation between FFOPI and FFP (R2 = 0.98); however, phantoms had a maximum fat fraction of 40%. Two previous studies [1, 5] using opposed-phase imaging in patients showed a good correlation between FFOPI and histologic fat score (r = 0.84-0.86), but opposed-phase imaging underestimated fat fraction in subjects with high histologic fat scores, likely related to the lack of resolution for fat-water ambiguity with opposed-phase imaging, as discussed by Levenson et al. [1]. 1H MRS allows the examination of the resonance frequencies of all protons within a volume of interest and can provide an accurate assessment of liver fat using commercially available software [7-11]. The number of protons contributing to a given spectral peak is directly proportional to the area under the peak. It allows in vivo quantitative evaluation of metabolites such as water and fat within a selected volume of interest. 1H MRS provides also a quick method with which to determine fat or water dominance for simple fat calculation using opposed-phase imaging.

However, 1H MRS is slightly more time consuming and operator dependent than opposed-phase imaging, with some degree of interobserver variability, and it evaluates only a portion of liver parenchyma. In addition, quantitative analysis requires the correction for signal decay from T2 relaxation. Signal saturation from incomplete T1 relaxation is minimized by using a long TR. Allowing for these corrections, Longo et al. [7, 9] studied a population of patients with liver steatosis and found a good correlation between fat fraction measured with 1H MRS and CT and the histologic results. In another study in patients with alcoholic steatosis, Thomsen et al. [8] reported a strong correlation between MRS and histology (r = 0.9).

Our study has some limitations: First, it included phantom data only, without correction for T2 decay; a clinical validation of the combined use of opposed-phase imaging with 1H MRS is needed. Second, qualitative analysis of opposed-phase images was performed by a single observer, who was a clinical fellow at that time and was interpreting opposed-phase images routinely.

The underlying mechanism of liver inflammation and fibrosis in nonalcoholic steatohepatitis is still unclear, and it has not been clearly proven that simple steatosis without associated inflammation or fibrosis increases the risk of liver damage. Despite these facts, opposed-phase imaging and 1H MRS could have important potential clinical applications by facilitating diagnosis and monitoring disease progression in a large population of patients including liver donors, obese patients, and diabetic patients and could obviate liver biopsy [5, 11-14].

In conclusion, an accurate estimation of fat fraction can be obtained using opposed-phase imaging with qualitative 1H MRS to resolve the ambiguity of fat or water dominance.


References
Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 

  1. Levenson H, Greensite F, Hoefs J, et al. Fatty infiltration of the liver: quantification with phase-contrast MR imaging at 1.5 T vs biopsy. AJR 1991; 156:307 -312[Abstract/Free Full Text]
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  6. Outwater EK, Blasbalg R, Siegelman ES, Vala M. Detection of lipid in abdominal tissues with opposed-phase gradient-echo images at 1.5 T: techniques and diagnostic importance. RadioGraphics1998; 18:1465 -1480[Abstract]
  7. Longo R, Ricci C, Masutti F, et al. Fatty infiltration of the liver: quantification by 1H localized magnetic resonance spectroscopy and comparison with computed tomography. Invest Radiol 1993; 28:297 -302[Medline]
  8. Thomsen C, Becker U, Winkler K, Christoffersen P, Jensen M, Henriksen O. Quantification of liver fat using magnetic resonance spectroscopy. Magn Reson Imaging 1994;12 : 487-495[CrossRef][Medline]
  9. Longo R, Pollesello P, Ricci C, et al. Proton MR spectroscopy in quantitative in vivo determination of fat content in human liver steatosis. J Magn Reson Imaging 1995;5 : 281-285[Medline]
  10. Szczepaniak LS, Nurenberg P, Leonard D, et al. Magnetic resonance spectroscopy to measure hepatic triglyceride content: prevalence of hepatic steatosis in the general population. Am J Physiol Endocrinol Metab 2005; 288:E462 -E468[Abstract/Free Full Text]
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