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Genitourinary Imaging |
1 From the Department of Radiology, Kumamoto University School of Medicine, 1-1-1 Honjo, Kumamoto 860-8556, Japan. Received January 5, 2000; revision requested February 22; revision received July 10; accepted July 25. Address correspondence to T.N. (e-mail: tomohiro@kaiju.medic.kumamoto-u.ac.jp).
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONAPPENDIXREFERENCES |
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MATERIALS AND METHODS: The study consisted of two parts: a phantom study and a clinical study. To explore the effect of the T1 value on in- and opposed-phase MR images of fat-containing tissues, phantom models with various proportions of fat and gadopentetate dimeglumine concentrations were implemented. Signal intensity (SI) indexes ([SI in-phase - SI opposed-phase]/SI in-phase) were calculated with double-echo fast low-angle shot (FLASH) MR imaging. In the clinical study, 23 patients with 28 adrenal masses (16 adrenal adenomas, nine adrenal metastases, and three pheochromocytomas) underwent double-echo FLASH MR imaging, and SI indexes were calculated.
RESULTS: SI index reached a maximum of 0.87 at 53% fat fraction for gadopentetate dimeglumine concentration at 0.5 mmol/L as the simulated T1 of the adrenal mass. The SI indexes of the adrenal adenomas, adrenal metastases, and pheochromocytomas, respectively, were 0.36, -0.15, and -0.07, and estimated fat fraction from the phantom study was 26.5%, 0%, and 0%. All adrenal adenomas contained fat on double-echo FLASH images. There was no overlap in SI index between adenomas and other tumors.
CONCLUSION: Preliminary experience indicates that quantitative measurement of the fat fraction of adrenal masses is possible with the double-echo chemical shift FLASH technique and allows for differentiating adrenal adenomas from other adrenal masses.
Index terms: Adrenal gland, MR, 86.121414, 86.121416 • Adrenal gland, neoplasms, 86.317, 86.328, 86.339 • Fat, MR, 86.121414, 86.121416 • Magnetic resonance (MR), chemical shift, 86.121414 • Magnetic resonance (MR), rapid imaging, 86.121416 • Phantoms, 86.121413
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONAPPENDIXREFERENCES |
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The purpose of this study was to quantify fat content within adrenal lesions on the basis of estimates from a phantom study and to differentiate adrenal adenomas from other adrenal masses by assessing fat content in a clinical study.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONAPPENDIXREFERENCES |
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T1 measurements of fat and various concentrations of gadopentetate dimeglumine (Magnevist; Schering, Berlin, Germany) in the phantoms were performed with an inversion-recovery spin-echo pulse sequence with a TR of 1,500 msec and inversion times of 10, 30, 80, 320, 640, and 1,280 msec. The field of view and imaging matrix were the same as those for the double-echo FLASH sequence.
Phantom Study
Because we used a short TR and short TEs, the apparent signal intensity fraction, f, was affected by the value of T1. Theoretically, the equations that relate gadopentetate dimeglumine concentration and fat to signal intensity (SI) for opposed-phase, SIOP, and for in-phase, SIIP, MR imaging are as follows: SIOP = |{fF exp(-TE/T2*F) [1 - exp(-TR/T1F)] sin
/[1 - cos exp(-TR/T1F)]} - {fW exp(-TE/T2*W) [1 - exp(-TR/T1W)] sin/[1 - cos exp(-TR/T1W)]}| and SIIP = {fF exp(-TE/T2*F) [1 - exp(-TR/T1F)] sin/[1 - cos exp(-TR/T1F)]} + {fW exp(-TE/T2*W) [1 - exp(-TR/T1W)] sin/[1 - cos exp(-TR/T1W)]}, where T1W, T2*W, and fW are the T1, T2*, and SI fraction for water protons, respectively. T1F, T2*F, and fF are the corresponding parameters for fat protons (13).
To explore the effect of T1 value on in- and opposed-phase MR images of fat-containing tissues, we used a phantom model with a gadolinium chelate and oil. The water mixed with various gadopentetate dimeglumine concentrations (0, 0.5, 1.0, and 5.0 mmol/L) was layered on corn oil (Nissin Corn-yu; Nissin, Tokyo, Japan), which provided an oil-water interface in which to test various fractions of fat to water. The 2-cm-thick section allowed various proportions of fat and water protons within each voxel (Fig 1).
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Quantitative measurements of SI changes between in-phase and opposed-phase images were computed as described in previous reports (3–5). The SI index was calculated as follows: SI index = (SIIP - SIOP)/SIIP, where SIIP is SI on in-phase images and SIOP is SI on opposed-phase images.
In-phase and opposed-phase images ideally would be obtained with theoretic TEs (eg, TE of 2.2 msec for opposed phase and 4.4 msec for in phase). This could not be achieved in our double-echo FLASH sequence owing to a constraint of the vendor-developed software. However, we confirmed that the difference between the double-echo sequence (TEs, 2.7 and 5.2 msec) and the two ideal echoes (TEs, 2.2 and 4.4 msec) was negligible (see Appendix).
Clinical Study
Patient selection.—Twenty-three consecutive patients (14 male and nine female patients; age range, 15–88 years; mean age, 51.3 years) with 28 adrenal masses detected with computed tomography (CT) or ultrasonography, and with either histologic or clinical confirmation, were enrolled in the study. All patients underwent MR imaging as requested by their clinicians. All adrenal masses were at least 1 cm in diameter (mean, 3.2 cm; range, 1.0–8.3 cm). There were 16 nonfunctioning adenomas in 13 patients, nine metastases in seven patients (from lung cancer in four patients, from esophageal carcinoma in two patients, and from colon cancer in one patient), and three pheochromocytomas in three patients.
The diagnosis of a benign or malignant adrenal lesion was made on the basis of all available clinical, radiologic, and pathologic data. In seven patients, nine adrenal masses were diagnosed as malignant on the basis of positive findings at pathologic examination (n = 3) or progressive enlargement of the mass on serial CT or MR images (n = 6) in the presence of a known primary tumor. In 13 patients, 16 adrenal masses were diagnosed as adenoma on the basis of findings at biopsy (n = 4) or stability of size on serial CT or MR images (n = 12) obtained at follow-up studies for a minimum of 1 year (mean follow-up, 16 months; range, 12–22 months). None of the 13 patients had a primary malignancy. All three pheochromocytomas were proved by means of surgical resection.
Image analysis.—Region-of-interest measurements were made in the enlarged adrenal gland by using an area as large as possible but not including the edge of the adrenal gland, which interfaces with surrounding retroperitoneal fat. All measurements were made by one investigator (T.N.), who was blinded to the clinical data. Quantitative measurements of SI change between in- and opposed-phase images were computed from these data as described in the phantom study. The SI index was calculated as follows: SI index = (SIIP-adrenal - SIOP-adrenal)/SIIP-adrenal.
The SI index reflects the fraction of SI loss on opposed-phase images compared with the SI on in-phase images. SI indexes between patients with adenomas and those with other tumors were compared by using the unpaired Student t test. A P value of less than .05 was considered to indicate a statistically significant difference.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONAPPENDIXREFERENCES |
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The fat fractions versus measured SI indexes with various gadopentetate dimeglumine concentrations and fat phantoms are plotted in Figure 2. The SI index reached maximum values of 0.75 (30% fat fraction), 0.87 (53% fat fraction), 0.89 (55% fat fraction), and 0.69 (58% fat fraction) for gadopentetate dimeglumine concentrations of 0, 0.5, 1.0, and 5.0 mmol/L, respectively.
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Clinical Study
The SI indexes of the adrenal adenomas, adrenal metastases, and pheochromocytomas were 0.36 ± 0.18 (SD), -0.15 ± 0.12, and -0.07 ± 0.08, respectively. The mean estimated fat fraction from the phantom study was 26.5% for adenomas (Fig 3) and 0% each for adrenal metastases (Fig 4) and pheochromocytomas (Fig 5). The SI index and estimated fat fraction of the three types of adrenal masses are presented in Figures 6 and 7, respectively. There was no overlap in SI index between adenomas and other tumors. The SI index of the adrenal adenomas was significantly higher than that of the other adrenal masses (P < .001). These results indicated 100% sensitivity (16 of 16 adenomas), 100% specificity (12 of 12 masses), and 100% accuracy (28 of 28 masses) for differentiation of adenomas from other tumors. All of the adrenal adenomas contained fat, whereas the other adrenal masses did not contain fat.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONAPPENDIXREFERENCES |
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Chemical shift MR imaging techniques, which are based on the difference in resonance frequency of water (–OH) and fat (–CH2–) protons, can conclusively demonstrate intratumoral fatty content (1,15). Chemical shift imaging uses the decrease in SI on opposed-phase images to differentiate adenomas from other adrenal masses. Most adrenal adenomas contain fat, whereas most malignant lesions of the adrenal gland (primary carcinomas or metastases) do not. The double-echo FLASH technique ensures that both in-phase and opposed-phase images are obtained from the same anatomic position, regardless of the patients’ ability to hold their breath. Therefore, apparent differences in contrast between corresponding images from in and opposed phases are not caused by an inconsistent influence of section misregistration but only by the chemical shift of the lesion. Thus, a reference tissue for quantitative correction, such as the spleen or liver, was not necessary for our study with the double-echo FLASH technique.
In our study, a short TR (150 msec) was chosen so that, as a consequence, the calculated fat fraction was somewhat T1 dependent (Fig 2). There was no quantitative correction for the possible confounding influence of T2* decay in this study. The finding that fat fractions computed with and those computed without the correction are typically within 1% of each other indicates that T2* effects generally do not limit clinical application of this method (13). As a result, variability in the apparent fat fraction because of variability in adrenal water T2* is likely to be small. We believe this degree of reliability is well within an acceptable range to make this a clinically applicable method. Leroy-Willig et al (1) reported fat fractions in adrenal masses of 16.4% ± 7.8 in adrenal adenoma and 1.5% ± 2.0 in malignant tumor in vitro (1). We are encouraged by the similarity of our results (26.5% for the adenomas and 0% for the other adrenal masses) to that of Leroy-Willig et al (1).
Our study with the double-echo FLASH technique may have several limitations. First, the opposed-phase images accurately reflected the difference in the water and fat signals, and it was not possible to identify whether the fat or the water was the dominant signal. The adrenal adenoma may contain less than 50% fat (1). Thus, we assumed that the fat fraction is always less than the water fraction. Second, in-phase and opposed-phase images would ideally be obtained with theoretic TEs (eg, TE of 2.2 msec for opposed-phase and 4.4 msec for in-phase images) with the double-echo FLASH technique. This could not be achieved in our double-echo FLASH sequence because of a constraint of the vendor-developed software. However, we confirmed that the difference between our double-echo technique and optimal echoes was small and can be negligible in clinical applications. Third, voxels at the interface of fat and water may show a marked loss of SI on opposed-phase images, which will cause the familiar "etching" artifact around the adrenal lesion, regardless of fat content. This is an intrinsic problem with the opposed-phase technique for very small lesions. Finally, a limitation of the chemical shift technique is that absence of fat does not always indicate malignancy. When chemical shift imaging does not convincingly reveal a fat component within an adrenal mass, other causes of benign adrenal enlargement, such as pheochromocytoma, hemorrhagic pseudocysts, or adenomas without fat, as well as malignant tumors, must be considered in the differential diagnosis.
In conclusion, our preliminary experience shows that quantitative measurement of the fat fraction of adrenal masses is possible with the double-echo chemical shift FLASH technique, which allows for differentiating adrenal adenomas from other adrenal masses. In comparison with the single-echo FLASH sequence, noteworthy advantages of this double-echo technique include the absence of section misregistration and the short acquisition time in a single breath hold.
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APPENDIX |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONAPPENDIXREFERENCES |
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The fat fraction versus measured SI index with the double-echo FLASH sequence (TEs at 2.7 and 5.2 msec) and two single-echo FLASH sequences (correct TEs at 2.2 and 4.4 msec) are plotted in Figure A1, which shows the similar SI profiles between TEs of the double-echo FLASH sequence and the desirable TEs. The SI index reached a maximum value of 0.86 for the double-echo FLASH sequence and 0.78 for the control sequences at the same fat fraction (53%).
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FOOTNOTES |
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Author contributions: Guarantor of integrity of entire study, Y.Y.; study concepts and design, T.N.; definition of intellectual content, K.M.; literature research, T.N.; clinical studies, Y.N., O.M.; experimental studies, T.N.; data acquisition, T.N.; data analysis, M.K.; manuscript preparation, T.N.; manuscript editing, Y.Y.; manuscript review, Y.Y., M.T.; manuscript final version approval, T.N.
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REFERENCES |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONAPPENDIXREFERENCES |
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= water (T1, 2,803 msec), 
= 0.5 mmol/L (T1, 504 msec), 
= 1.0 mmol/L (T1, 292 msec), 
= 5.0 mmol/L (T1, 175 msec).
= adenoma, 
= metastasis, 
