Characterization of Adrenal Lesions at Chemical-Shift MRI: A Direct Intraindividual Comparison of In- and Opposed- Phase Imaging at 1.
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1 Genitourinary Imaging Original Research Ream et al. In- and Opposed-Phase Chemical-Shift 1.5 T and 3 T MRI of Adrenal Lesions Genitourinary Imaging Original Research Justin M. Ream 1 Byron Gaing 1 Thais C. Mussi 1,2 Andrew B. Rosenkrantz 1 Ream JM, Gaing B, Mussi TC, Rosenkrantz AB Keywords: adrenal glands, chemical-shift imaging, MRI DOI: /AJR Received March 30, 2014; accepted after revision May 13, Presented in part at the 2014 annual meeting of the International Society of Magnetic Resonance in Medicine, Milan, Italy. 1 Department of Radiology, Center for Biomedical Imaging, NYU School of Medicine, NYU Langone Medical Center, 660 First Ave, 3rd Fl, New York, NY Address correspondence to J. M. Ream (Justin.Ream@nyumc.org. 2 Present address: Hospital Israelita Albert Einstein, Sao Paolo-SP, Brazil. AJR 2015; 204: X/15/ American Roentgen Ray Society Characterization of Adrenal Lesions at Chemical-Shift MRI: A Direct Intraindividual Comparison of In- and Opposed- Phase Imaging at 1.5 T and 3 T OBJECTIVE. The purpose of this article is to perform an intraindividual comparison between 1.5 T and 3 T chemical-shift MRI in differentiating adrenal adenomas and nonadenomas, including comparison of quantitative thresholds. MATERIALS AND METHODS. In this retrospective study, 37 adrenal lesions in 36 patients (20 men and 16 women; mean [± SD] age, 66.7 ± 12.9 years; 27 benign adenomas in 27 patients; 10 nonadenomas in nine patients imaged at 1.5 T and 3 T were identified. Two readers qualitatively assessed intralesional signal loss between in- and opposed-phase images. One reader placed ROIs on adrenal lesions, spleen, liver, and muscle. Quantitative measures of signal loss, such as signal intensity (SI index, adrenal-to-spleen ratio, adrenal-to-liver ratio, and adrenal-to-muscle ratio, were calculated. Qualitative and quantitative measures between field strengths were assessed with McNemar test and ROC analysis, respectively. RESULTS. Accuracy in qualitative adenoma identification (86.5% [32/37] at 1.5 T and 81.1% [30/37] at 3 T for reader 1; 81.1% [30/37] at 1.5 T and 83.8% [31/37] at 3 T for reader 2; both p was equivalent at both field strengths. AUCs were not statistically significantly different between field strengths for quantitative measures: AUCs at 1.5 T versus 3 T were versus for SI index, versus for adrenal-to-spleen ratio, versus for adrenal-to-liver ratio, and versus for adrenal-to-muscle ratio (all p > The optimal threshold for SI index was lower at 3 T (> 7.4% than at 1.5 T (> 21.6% but had similar sensitivity (1.5 T, 92.6% [25/27]; 3 T, 88.9% [24/27] and specificity (1.5 T, 90.0% [9/10]; 3 T, 90.0% [9/10]. CONCLUSION. Chemical-shift imaging has similar diagnostic efficacy for differentiating adrenal adenomas and nonadenomas at 1.5 T and 3 T. However, quantitative measures have different thresholds for this differentiation at 3 T; in particular, the commonly applied SI index is much lower at 3 T. T he use of T1-weighted chemicalshift MRI for characterization of adrenal lesions is well established [1 3]. Chemical-shift MRI exploits the differences in precessional frequency between lipid and water protons. By assessing differences in signal intensity (SI at TEs when lipid and water protons within a single voxel are in phase versus are opposed phase, chemical-shift MRI allows the detection of the intracytoplasmic lipid [4] characteristic of most adrenal adenomas and, thus, the differentiation of benign adenomas and nonadenomas in most cases. The vast preponderance of published literature has evaluated chemical-shift imaging of adrenal lesions at an MRI field strength of 1.5 T. However, several key differences between 1.5 T and 3 T chemical-shift imaging exist. First, at 3 T, the doubling of field strength effectively doubles the differences in precessional frequency between lipid and water protons relative to that at 1.5 T [5]. Although this may allow greater separation of water and lipid protons, it also requires the selection of different TE pairs [6]. This selection of different TE pairs alters the separation between the in- and opposed-phase time points, which can lead to technical difficulty acquiring consecutive in- and opposed-phase echoes and also alter the contribution of T2* effects to the differences in SI between the in- and opposed-phase images. Furthermore, changing the magnetic field strength leads to inherent tissue-specific differences in T1 relaxation time [7]. These dif- 536 AJR:204, March 2015
2 In- and Opposed-Phase Chemical-Shift 1.5 T and 3 T MRI of Adrenal Lesions ferences in chemical-shift imaging between field strengths may limit the application of established quantitative signal loss thresholds derived from studies performed at 1.5 T to clinical imaging performed at 3 T and may also affect the accuracy of the technique in differentiating benign adenomas and nonadenomas at 3 T. A small number of reports have shown the efficacy of chemical-shift MRI for characterizing adrenal lesions at 3 T [6, 8 11]. However, there has been minimal direct comparison of adrenal lesion characterization between 1.5 T and 3 T. To our knowledge, only a single study [10] reports a comparison of 1.5 T and 3 T chemical-shift imaging for characterizing adrenal lesions. However, the data in that earlier study pertaining to differentiation of adenomas and nonadenomas were obtained in different patient groups at 1.5 T and 3 T, with only a small subset of adenomas (and no nonadenomas being evaluated at both field strengths. Thus, a direct intraindividual comparison of chemical-shift MRI in differentiating adenomas and nonadenomas at 1.5 T and 3 T has not been published. Therefore, the purpose of our study is to perform an intraindividual comparison of the efficacy of 1.5 T and 3 T chemical-shift MRI in the characterization of adrenal lesions, including a comparison between field strengths of quantitative thresholds for the differentiation of adenomas and nonadenomas. Materials and Methods Patient Population The retrospective study was HIPAA compliant and approved by the New York University School of Medicine institutional review board. A waiver of written informed consent was obtained. A departmental database was searched to identify abdominal MRI examinations performed between January 2007 and September 2013 in which the report contained any of the following phrases (including the plural form of each: adrenal adenoma, adrenal mass, adrenal lesion, adrenal metastasis, or adrenal tumor. This search identified 871 patients who had at least one report that mentioned any of the target phrases. The records of these patients were then further assessed for the presence of separate abdominal MRI examinations studies performed at 1.5 T and 3 T, yielding 83 adrenal lesions in 81 patients. Among these patients, adrenal cysts (n = 2 and lesions containing bulk fat (indicative of myelolipoma, n = 2 were excluded because chemicalshift MRI is generally not used for further characterization of such lesions. Lesions measuring 0.7 cm or less in maximum dimension (n = 3 were also excluded because of difficulty in accurately placing an ROI in lesions of this size. Among the remaining cases, 28 lesions in 27 patients were excluded because of the use of a routine clinical imaging protocol that was not standardized for evaluation of adrenal lesions. In addition, 11 lesions in 11 patients were excluded because of a lack of an adequate reference standard. These exclusions left a final cohort of 37 lesions in 36 patients (20 men and 16 women; mean [± SD] age, 66.7 ± 12.9 years. Study inclusions and exclusions are summarized in Figure 1. Initial search 871 patients with adrenal lesion mentioned in MRI report Eligible patients 83 lesions in 81 patients with adrenal lesions imaged at both 1.5 T and 3 T Final study population 37 lesions in 36 patients Adrenal adenomas 27 lesions in 27 patients Nonadenomas 10 lesions in 9 patients Fig. 1 Flowchart of study inclusions and exclusions. Clinical Reference Standard A lesion was classified as a benign adrenal adenoma on the basis of imaging stability (< 10% change in size over a minimum of 1 year [12 14] (n = 9, unenhanced CT attenuation values of less than 10 HU [15] (n = 2, or both (n = 16. A lesion was classified as a nonadenoma according to either pathologic proof (seven lesions in seven patients or rapid growth (defined as 30% growth in maximum diameter over 6 months [8]; n = 3 lesions in two patients. A total of 27 lesions (mean diameter, 1.6 ± 0.6 cm in 27 patients met criteria for benign adenomas. A total of 10 lesions in nine patients (mean diameter, 2.8 ± 2.2 cm met criteria for nonadenomas. Among the nonadenomas, eight lesions in seven patients were metastases from a known primary malignancy, including four metastases from hepatocellular carcinoma in three patients (one of which was pathologically proven after surgical resection, and three of which showed rapid growth on serial imaging as defined already, three metastases from lung cancer in three patients (two of which were pathologically proven after surgical resection and one of which met growth criteria, and one pathologically proven metastasis from a retroperitoneal sarcoma. The remaining two nonadenomas were primary neoplasms of the adrenal gland, including a neurogenic tumor and a pheochromocytoma, both of which were pathologically proven after surgical resection. All MRI examinations were performed as part of routine clinical practice. In 28 patients (including one patient with two lesions, both 1.5 T and 3 T examinations were performed for surveillance of a known neoplasm. Other clinical indications for the examinations included liver evaluation in the setting of cirrhosis (two patients, monitoring of pancreatic cysts (two patients, monitoring of adrenal lesions (two patients, surveillance imaging in the setting of multiple endocrine neoplasia type 2 (one patient, surveillance imaging in the setting of tuberous sclerosis (one patient, and follow-up of retroperitoneal fibrosis (one patient. MRI MRI at 1.5 T was performed on one of several systems (Magnetom Symphony [n = 13], Magnetom Avanto [n = 13], Magnetom Sonata Vision Insufficient imaging 790 patients imaged at only one field strength Excluded patients 46 lesions in 45 patients Nonstandard imaging protocol: 28 lesions in 27 patients Inadequate proof of diagnosis: 11 lesions in 11 patients Small lesion size ( 7 mm: 3 lesions in 3 patients Adrenal cysts: 2 lesions in 2 patients Adrenal myelolipomas: 2 lesions in 2 patients AJR:204, March
3 Ream et al. [n = 10], and Magnetom Aera [n = 1]; all from Siemens Healthcare. The in- and opposed-phase sequences were acquired in a single breath-hold using an axial 2D gradient-echo T1-weighted sequence with in-phase TE of ms and opposed-phase TE of ms. These TEs correspond with the first in- and opposed-phase echoes. Other sequence parameters varied given the use of multiple scanners at both field strengths as well as the nearly 7-year duration of the study; representative parameters are as follows: matrix, ; FOV, mm with 80% rectangular FOV (adjusted according to the patient s body size; flip angle, 80 ; and TR, ms. MRI at 3T was performed on one of two systems (Magnetom Trio TIM [n = 34] or Magnetom Verio [n = 3]; both from Siemens Healthcare. In- and opposed-phase sequences were acquired in a single breath-hold using a 2D gradient-echo sequence. In-phase images were acquired at the second in-phase resonance frequency at 3 T (actual TE, 4.40 ms for all studies, and opposedphase images were acquired near the first 3 T opposed-phase peak of 1.1 ms (actual TE, 1.55 ms for all studies. These TEs correspond to the first opposed-phase and second in-phase echoes; this combination reflects a standard approach to performing chemical-shift MRI at 3 T in current clinical practice given the challenge in obtaining consecutive in- and opposed-phase TEs relating to their closer temporal spacing compared with at 1.5 T. Additional representative scanning parameters include the following: matrix, ; FOV, mm with 80% rectangular FOV (adjusted according to the patient s body size; flip angle, 80 ; and TR, ms. TR was slightly greater at 3 T than at 1.5 T, reflecting the slower T1 recovery at 3 T. Image Analysis Analysis was performed on an image analysis workstation (Leonardo, Siemens Healthcare. Qualitative analysis was performed by two observers (with 1 and 6 years of experience in abdominal MRI, respectively. Readers were blinded to both the diagnosis and the imaging parameters (including the scanner field strength. The studies were evaluated in a random order, with 1.5 T and 3 T examinations intermixed. For each lesion, readers viewed in- and opposed-phase images at corresponding slices at the level of the target adrenal lesion on a single screen and made a qualitative binary determination of whether there was visual loss of signal within the lesion between in- and opposed-phase images. Quantitative analysis was performed by reader 1 after a training session in which the reader was familiarized with the software and was trained in ROI placement for two sample patients. For each lesion, in- and opposed-phase images were viewed on the same screen. A freehand ROI was placed in the adrenal lesion on the opposed-phase image and was drawn as large as possible to include the entire lesion but excluding the lesion s edge. The ROI was then copied and pasted onto the same slice on the in-phase image. The mean and SD of the SI were recorded for both images. This process was performed twice for each lesion, and the SI was averaged between the two ROIs. The second ROI was placed on a different slice if possible; if the lesion was present on only a single slice, then the reader deleted the original ROI and placed the second ROI on the same slice. Additional reference ROIs were drawn in each case within the liver, spleen, and paraspinal muscle. These were placed on the same slice as the adrenal lesion ROI while avoiding vessels, organ edges, adjacent nontarget tissues (e.g., fat or bone, or artifact. If the reference ROI could not be drawn on the same slice as the adrenal lesion, then it was drawn on the nearest possible slice. As with the adrenal lesions, two separate ROIs were drawn in each reference organ. On the basis of these ROI data, four quantitative indexes of signal change between in-phase (IP and opposed-phase (OP images were calculated [16] as follows: SI index = (SI adrenal IP - SI adrenal OP 100% SI adrenal IP (1. Adrenal-to-spleen ratio= (SI adrenal OP SI spleen OP % (SI adrenal IP SI spleen IP Adrenal-to-muscle ratio= (SI adrenal OP SI muscle OP % (SI adrenal IP SI muscle IP Adrenal-to-liver ratio= (SI adrenal OP SI liver OP (SI adrenal IP SI liver IP 100% -1 (2, (3, (4. Statistical Analysis The McNemar test was used to compare the sensitivity and accuracy of subjective signal loss for differentiation of adrenal adenomas and nonadenomas between 1.5 T and 3 T. ROC analysis was performed for each of the four quantitative metrics (SI index, adrenal-to-spleen ratio, adrenal-to-muscle ratio, and adrenal-to-liver ratio at both 1.5 T and 3 T. One patient with an adrenal adenoma had diffuse hepatic steatosis (73% signal loss between in- and opposed-phase images at 1.5 T and was excluded from the adrenal-to-liver ratio ROC analysis; none of the other examinations showed more than 7% signal loss between in- and opposed-phase sequences. In addition, pairwise comparison of ROC curves was performed for each of the four quantitative ratios between 1.5 T and 3 T. Optimal thresholds were identified for each combination of ratio and field strength, defined as the threshold maximizing the average of sensitivity and specificity. All p values are two-sided and are considered statistically significant at p < Analysis was performed using software (MedCalc for Windows, version 12.7, MedCalc Software. Results On the basis of visual assessment of perceived signal loss between in- and opposedphase images (Table 1, there was no statistically significant difference between 1.5 T and 3 T for accuracy (reader 1, 86.5% vs 81.1%; reader 2, 81.1% vs 83.8%, sensitivity (reader 1, 85.2% vs 81.5%; reader 2, 85.2% vs 85.2%, or specificity (reader 1, 90.0% vs 80.0%; reader 2, 70.0% vs 80.0% for differentiation of adrenal adenomas and nonadenomas (all p Quantitative metrics of signal loss generally had sensitivities and specificities similar to those of visual assessment in differentiating adenomas from nonadenomas at both 1.5 T and 3 T (Tables 1 and 2. AUC values for quantitative metrics ranged from to AUC values for SI index showed no statistically significant difference between 1.5 T and 3 T (0.956 vs 0.915; p = The calculated optimal threshold for differ- TABLE 1: Comparison Between 1.5 T and 3 T of Performance of Subjective Signal Loss for Differentiation of Adrenal Adenomas and Nonadenomas 1.5 T 3 T Reader Accuracy Sensitivity Specificity Accuracy Sensitivity Specificity Reader (32/ (23/ (9/ (30/ (22/ (8/10 Reader (30/ (23/ (7/ (31/ (23/ (8/10 Note Data are percentage (no. of lesions/total. 538 AJR:204, March 2015
4 In- and Opposed-Phase Chemical-Shift 1.5 T and 3 T MRI of Adrenal Lesions TABLE 2: Comparison Between 1.5 T and 3 T of Performance of Quantitative Chemical-Shift Metrics for Differentiation of Adrenal Adenomas and Nonadenomas 1.5 T 3 T Metric AUC entiating adenomas and nonadenomas was markedly lower at 3 T than at 1.5 T for SI index (Fig. 2. Specifically, the optimal threshold was 26.1% signal loss at 1.5 T and 7.4% signal loss at 3 T, which yielded similar sensitivities (92.6% at 1.5 T vs 88.9% at 3 T and specificities (90.0% at 1.5 T vs 90.0% at 3 T. No statistically significant difference was found between 1.5 T and 3 T for the AUC for adrenal-to-spleen ratio (0.963 vs 0.870; p = 0.133, adrenal-to-liver ratio (0.935 vs 0.852; p = 0.118, and adrenal-to-muscle ratio (0.948 vs 0.948; p = For adrenal-to-spleen ratio and adrenal-to-liver ratio, absolute optimal thresholds at 3 T were lower than those at 1.5 T (adrenal-to-spleen ratio, threshold of 17.2% at 3 T vs 35.9% at 1.5 T; adrenalto-liver ratio, threshold of 24.5% at 3 T vs 32.6% at 1.5 T, whereas for adrenalto-muscle ratio, the absolute optimal threshold at 3 T was higher than at 1.5 T ( 39.6% at 3 T vs 29.3% at 1.5 T. Both adrenalto-spleen ratio and adrenal-to-muscle ratio had similar sensitivities and specificities between 3 T and 1.5 T at the optimal thresholds (adrenal-to-spleen ratio, sensitivity of 85.2% and specificity of 90.0% at 3 T, vs sensitivity of 92.6% and specificity of 90.0% at 1.5 T; adrenal-to-muscle ratio, sensitivity of 88.9% and specificity of 90.0% at 3 T versus sensitivity of 92.6% and specificity of 90.0% at 1.5 T. Adrenal-to-liver ratio exhibited a sensitivity and specificity of 76.9% and 100.0%, respectively, at 3 T, compared with 92.3% and 90.0%, respectively, at 1.5 T. Discussion Our study shows comparable performance between 1.5 T and 3 T chemical-shift imaging in the differentiation of adrenal adenomas and nonadenomas. Specifically, there was no statistically significant difference between field strengths with regard to accuracy for either of two readers based on subjective signal loss or for the AUC of any of Optimal Threshold (% Sensitivity a Specificity a AUC Optimal Threshold (% Sensitivity a Specificity a Signal intensity index > (25/ (9/ > (24/ (9/10 Adrenal-to-spleen ratio (25/ (9/ (23/ (9/10 Adrenal-to-liver ratio (24/ (9/ (20/ (10/10 Adrenal-to-muscle ratio (25/ (9/ (24/ (9/10 a Data are percentage (no. of lesions/total. four quantitative ROI-based chemical-shift metrics. These results indicate that, despite the doubling of the difference in precessional frequency between lipid and water protons at 3 T and the associated more rapid in- and opposed-phase cycling of these at 3 T, it remains possible to reliably characterize adrenal lesions at the higher field strength. These findings are important given the increasing use of 3-T systems by many practices and the need to select the most appropriate equipment for examinations of a given indication. There was a paucity of data on this topic before our current study. Several past studies reported data regarding the performance of 3 T MRI for characterizing adrenal lesions [8 10, 17]. Only one of those studies attempted a comparison with 1.5 T [10], but only the adenoma subset was imaged at both 1.5 T and 3 T, such that findings regarding differentiation of adenomas and nonadenomas were based on different patient groups imaged at 1.5 T and 3 T. Given the variable lipid content present in adrenal adenomas [18] and the sensitivity of chemical-shift imaging to the amount of lipid deposition [19], this comparison benefits from a true intraindividual assessment, as is achieved by our study. Although the overall performance of chemical-shift imaging was similar at the two field strengths, the differences in the physical properties of protons at different field strengths did affect the optimal thresholds for the quantitative measures of signal loss between in- and opposed-phase images at 1.5 T and 3 T. Two prior studies [8, 10] have suggested that the SI index is the most reliable parameter for differentiating adenomas from nonadenomas at 3 T when the in-phase TE is longer than that of the opposed-phase TE. In our study, although SI index had similar performance at 1.5 T and 3 T, the threshold for signal loss was much lower at 3 T (> 7.4% than at 1.5 T (> 26.1%. Thus, it is important for radiologists to be aware of these differences when using chemical-shift imaging to characterize adrenal lesions, so as to avoid misinterpretations. Using the other quantitative measures, all of which were indexed to other tissues, sensitivity and specificity were also similar between 1.5 T and 3 T, although the relationships of the thresholds between field strengths were less consistent. There are several limitations of this study. First, our qualitative and quantitative assessments depended on the presence of microscopic lipid (as evidenced by loss of signal between in- and opposed-phase images as a marker of benign adrenal adenomas. However, a distinct minority of benign adenomas are known to contain little or no intracytoplasmic lipid [20]. Thus, although these quantitative thresholds provide a relatively sensitive marker for the detection of intracellular lipid, lesions that do not reach these thresholds should be viewed in light of this possibility, and other imaging features that have been shown to effectively characterize these lipid-poor adenomas (e.g., CT washout characteristics [21] should be considered. In addition, several reports have shown the presence of microscopic lipid within adrenal metastases from primary neoplasms that may also contain microscopic lipid, such as clear cell renal cell carcinomas [22] and hepatocellular carcinoma [23]. Thus, caution is warranted when applying the quantitative thresholds derived from the current data to adrenal lesions in patients with such primary lesions. Also, in- and opposed-phase images were obtained at 3 T using TEs of approximately 4.4 ms and 1.1 ms, respectively. Although this represents a widely implemented approach to chemical-shift imaging at 3 T in clinical practice today [5, 6, 24], the use of other TE pairs has also been reported at 3 T [5]; in particular, the use of the first TE pair of approximately 2.2 and 1.1 ms at 3 T, which previously was difficult because of AJR:204, March
5 Ream et al. A C Fig year-old woman with an incidentally detected adrenal adenoma, which was stable over several years of imaging. Axial 2D gradient-echo T1-weighted MRI was performed. A and B, In-phase (A and opposed-phase (B 1.5 T images (in-phase TE, 4.76 ms; opposed-phase TE, 2.38 ms show diffuse homogeneous subjective signal loss within the adenoma (arrow, with a signal intensity index of 62%. C and D, In-phase (C and opposed-phase (D 3 T images (in-phase TE, 4.40 ms; opposed-phase TE, 1.55 ms show a lesser degree of subjective signal loss, with a much lower signal intensity index of 26%. Adenoma is indicated by arrow. hardware limitations of early 3 T MRI systems, has become increasingly implemented in clinical practice. Presumably, the use of alternate TE pairs may further affect the signal change between in- and opposed-phase images, and additional investigation is needed to establish thresholds for signal loss using these other combinations. B D The sample size was small, particularly of nonadenomas. However, many such lesions are surgically resected and do not undergo serial MRI evaluation. We do note that our number of nonadenomas was larger than in earlier studies of chemical-shift imaging of adrenal lesions at 3 T [8, 18]. In addition, we used as our reference standard for adenomas a combination of stability in size for a period of at least 1 year and established unenhanced CT criteria in the diagnosis of benign adenomas rather than histologic confirmation. However, suspected adrenal adenomas typically do not warrant histologic confirmation. Both size stability [8, 10, 12 14, 17, 25, 26] and unenhanced CT criteria [8, 18, 27, 28] have been widely used as reference standards for adrenal adenomas; indeed, past literature has largely used a shorter period of stability of 6 months [8, 10, 17] as criteria for benign adenoma, such that our requirement for 12-month stability provides a greater level of certainty of the benign nature of these lesions. Finally, our derived thresholds for SI index and adrenal-to-spleen ratio at 1.5 T differ somewhat from those generally applied in the literature (SI index of 16.5% and adrenalto-spleen ratio of 0.71; however, those widely used values have been propagated largely on the basis of a single study [16]. In conclusion, this study provides the first reported intraindividual comparison of the performance of chemical-shift MRI to differentiate adenomas and nonadenomas between 1.5 and 3 T. Although overall performance between 1.5 and 3 T is similar using both qualitative and quantitative approaches, the optimal thresholds for determining the presence of signal loss using quantitative measures must be adjusted at 3 T. Of note, a substantially lower threshold is required at 3 T when using the commonly applied SI index. Radiologists awareness of these findings is important when attempting to characterize adrenal lesions using chemical-shift MRI at different field strengths. References 1. Israel GM, Korobkin M, Wang C, Hecht EN, Krinsky GA. Comparison of unenhanced CT and chemical shift MRI in evaluating lipid-rich adrenal adenomas. AJR 2004; 183: Namimoto T, Yamashita Y, Mitsuzaki K, et al. Adrenal masses: quantification of fat content with double-echo chemical shift in-phase and opposed-phase FLASH MR images for differentiation of adrenal adenomas. Radiology 2001; 218: AJR:204, March 2015
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