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1 Department of Radiology, NYU Medical Center, 560 First Ave., Ste. HW 202, New
York, NY 10016.
2 Department of Radiology, University of Michigan, 1500 E Medical Center Dr.,
Ann Arbor, MI 48109-0030.
Received October 30, 2003;
accepted after revision January 6, 2004.
Address correspondence to G. M. Israel
(gary.israel{at}med.nyu.edu).
Abstract
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MATERIALS AND METHODS. Between January 1999 and June 2003, 40 patients (42 adrenal masses) underwent unenhanced CT and chemical shift MRI and were retrospectively analyzed. Hounsfield units, adrenal-to-spleen chemical shift ratio, and signal-intensity index were obtained for each adrenal mass. Qualitative analysis for loss of signal in each adrenal mass on the opposed-phase images was also performed by two reviewers and compared with the quantitative analyses. A lipid-rich adenoma was diagnosed if the mass measured equal to or less than 10 H, had an adrenal-to-spleen chemical shift ratio of less than 0.71, and had a signal-intensity index of greater than 16.5% or if the mass fulfilled two of the preceding criteria and had follow-up imaging without change.
RESULTS. The sensitivities and specificities for diagnosing a lipid-rich adenoma using the qualitative, adrenal-to-spleen chemical shift ratio, signal-intensity index, and unenhanced CT attenuation analyses were 92% (33/36) and 17% (1/6), 100% (36/36) and 100% (6/6), 100% (36/36) and 67% (4/6), and 78% (28/36) and 83% (5/6), respectively. Twenty-eight (67%) lipid-rich adenomas measured equal to or less than 10 H, had an adrenal-to-spleen chemical shift ratio of less than 0.71, and had a signal-intensity index of greater than 16.5%. Eight masses (19%) measured greater than 10 H but had an adrenal-to-spleen chemical shift ratio of less than 0.71 and a signal-intensity index greater than 16.5% and were unchanged at follow-up.
CONCLUSION. Eight (62%) of 13 adrenal adenomas measuring greater than 10 H on unenhanced CT were definitively characterized with chemical shift MRI.
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The CT scans and MR images were reloaded onto a PACS (picture archiving and communication system). For CT, one author manually defined a circular or oval region-of-interest (ROI) measurement in the center of the adrenal mass to obtain Hounsfield unit measurements. For the MR images, signal-intensity measurements were obtained using a manually defined ROI placed in the center of the adrenal mass and spleen on both in-phase and opposed-phase images. In one patient (one adrenal mass) who had undergone splenectomy, the left kidney was used for signal-intensity measurement instead of the spleen. For the adrenal masses, the largest ROI was placed that did not include partial volume effects from the adjacent fat or from the India ink artifact present on opposed-phase MR images. For the splenic ROI measurements, large blood vessels were avoided. An adrenal-to-spleen chemical shift ratio and a signal-intensity index were calculated. The adrenal-to-spleen chemical shift ratio was defined as the adrenal mass–to-spleen signal-intensity ratio on the opposed-phase images divided by the adrenal mass–to-spleen signal-intensity ratio on the in-phase images. The signal-intensity index was defined as the adrenal mass signal intensity on the in-phase images minus the adrenal mass signal intensity on the opposed-phase images divided by the adrenal mass signal intensity on the in-phase images multiplied by 100%.
Two independent radiologists (with 2 and 10 years' experience in interpreting abdominal MR images) who were blinded to the quantitative data reviewed the in- and opposed-phase images for the presence or absence of qualitative signal loss in the adrenal mass using the spleen (kidney, n = 1) as a reference. Any discrepancy between the two radiologists was settled by consensus. A comparison of the quantitative and qualitative results was performed.
All CT examinations were performed on helical scanners (HiSpeed Advantage [n = 15] or CTi [n = 16], General Electric Medical Systems; Volume-Zoom [n = 9], Siemens Medical Solutions). The slice collimation varied (10 mm, n = 1; 7 mm, n = 15; 5 mm, n = 21; 3 mm, n = 1; and 1.25 mm, n = 2). For the 23 masses that measured less than 1.5 cm, the mean slice collimation was 5.6 mm.
All MRI examinations were performed on a 1.5-T system (Vision or Symphony, Siemens Medical Solutions) using a torso phased array coil. All patients underwent axial breath-hold dual-echo T1-weighted imaging (in-phase and opposed-phase) using a 2D gradient-refocused echo sequence. The TR range was 152–200 and the TE ranges were 2.1–2.7 (opposed-phase) and 4.8–5.3 (in-phase). Other imaging parameters were as follows: matrix, 128 x 256; slice thickness, 4–8 mm; interslice gap, 0.6–2 mm; and rectangular field of view, 200–263 x 320–375 mm.
The final diagnosis of each mass was based on the available radiologic and pathologic data. The diagnosis of a lipid-rich adenoma was made if the mass measured equal to or less than 10 H on unenhanced CT [7], had an adrenal-to-spleen chemical shift ratio of less than 0.71 on MRI [5], and had a signal-intensity index of greater than 16.5% [8] or if the mass fulfilled two of the three preceding criteria and had greater than 6-month imaging follow-up without any interval change. If a mass did not meet the criteria of a lipid-rich adenoma but had imaging follow-up of 1 year or more without change, it was considered benign.
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Quantitative Analysis
Of the 42 adrenal masses, 28 (67%) measured less than or equal to 10 H on
unenhanced CT, had an adrenal-to-spleen chemical shift ratio of less than
0.71, and a signal-intensity index of greater than 16.5% (Figs.
1 and
2), consistent with lipid-rich
adrenal adenomas. The mean CT attenuation was –1.0 H (range, –23.1
to 10 H), the mean adrenal-to-spleen chemical shift ratio was 0.47 (range,
0.18–0.70), and the mean signal-intensity index was 56.6% (range,
26–83%).
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Eight masses (19%) measured greater than 10 H on unenhanced CT but had an adrenal-to-spleen chemical shift ratio of less than 0.71 and a signal-intensity index of greater than 16.5% (Fig. 3A, 3B, 3C). The mean unenhanced CT attenuation, adrenal-to-spleen chemical shift ratio, and signal-intensity index were the following: 19 H (range, 14.1–26 H), 0.50 (range, 0.32–0.67), and 49% (range, 28–68%), respectively. The mean follow-up time for these masses was 2.6 years (range, 6 months–5 years). No change in size was seen in of any of these masses, and they were consistent with lipid-rich adrenal adenomas.
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Two masses (5%) measured greater than 10 H on unenhanced CT and had an adrenal-to-spleen chemical shift ratio of greater than or equal to 0.71 but had a signal-intensity index of greater than 16.5%. The mean unenhanced CT attenuation, adrenal-to-spleen chemical shift ratio, and signal-intensity index were 18.8 H (range, 16.7–20.9 H), 0.75 (range, 0.73–0.76), and 33.5% (range, 27–40%), respectively. These masses were unchanged in size with a mean follow-up time of 1.9 years (range, 1.4–2.4 years) and were considered benign.
Three masses (7%) measured greater than 10 H on unenhanced CT, had an adrenal-to-spleen chemical shift ratio of greater than or equal to 0.71, and had a signal-intensity index of less than 16.5%. The mean CT attenuation, adrenal-to-spleen chemical shift ratio, and signal-intensity index were 33.6 H (range, 21.1–40.0 H), 1.0 (range, 0.84–1.1), and 7.1% (range, 1–16.2%), respectively. One of these masses measured 39.7 H on unenhanced CT, had an adrenal-to-spleen chemical shift ratio of 1.07 and a signal-intensity index of 4%, and was found to be a pheochromocytoma at surgery. The two remaining masses were unchanged in size with a mean follow-up time of 2.6 years (range, 2–3.2 years) and were considered benign.
A single mass (2%) measured –8 H on unenhanced CT but had an adrenal-to-spleen chemical shift ratio of 1.01 and a signal-intensity index of 0%. This mass was unchanged at 1-year follow-up and was considered benign.
Overall, chemical shift MRI characterized eight (62%) of 13 adrenal masses that measured greater than 10 H on unenhanced CT as lipid-rich adrenal adenomas.
Qualitative Analysis
The qualitative analysis was concordant with all three quantitative
evaluations in 27 (64%) of 42 adrenal masses, whereas in 15 masses (36%), it
was discordant with at least one of the quantitative evaluations
(Table 1). In two (13%) of
these 15 masses (masses 1 and 2 on Table
1), all three quantitative parameters characterized a lipid-rich
adenoma, but the qualitative analysis did not identify visual signal loss. In
two (13%) of 15 masses (masses 3 and 4) in which qualitative signal loss was
identified, a lipid-rich adenoma was not diagnosed by any of the three
quantitative measures. In eight (53%) of 15 masses (masses 5–12), the
adrenal-to-spleen chemical shift ratio and signal-intensity index
characterized a lipid-rich adenoma, but all these masses measured greater than
10 H on unenhanced CT. In one of these cases (mass 5), the qualitative
analysis did not identify signal loss, whereas in the remaining seven cases
(masses 6–12), qualitative signal loss was identified. These eight
masses were stable at follow-up (mean, 2.5 years; range, 6 months–5
years) and were consistent with lipid-rich adenomas. In three of 15 masses
(masses 13–15), qualitative analysis identified signal loss; however,
only one of the quantitative analyses (signal-intensity index [n = 2]
and unenhanced CT [n = 1]) met the criteria of a lipid-rich adenoma.
These three masses were stable at follow-up (mean, 1.6 years; range,
1–2.4 years).
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This study shows that eight (62%) of 13 lipid-rich adenomas could be characterized using chemical shift MRI when unenhanced CT values were greater than 10 H. Outwater et al. [5] performed a similar study using the same adrenal-to-spleen chemical shift ratio, which showed a high correlation between the unenhanced CT attenuation of adrenal masses and the adrenal-to-spleen chemical shift ratio. Similar to our results, their study also uncovered three benign adrenal masses (presumed lipid-rich adenomas) that measured greater than 10 H on unenhanced CT and had adrenal-to-spleen chemical shift ratios of less than 0.71, supporting the notion that chemical shift MRI is more sensitive for the diagnosis of a lipid-rich adrenal adenoma. However, a single malignant lesion in their study with an adrenal-to-spleen chemical shift ratio of 0.70 was misclassified as benign.
A similar study by McNicholas et al. [6] also compared unenhanced CT and chemical shift MRI in evaluating adrenal masses. They used the same adrenal-to-spleen chemical shift ratio and threshold on MRI as those used in this study but used a lower threshold (0 H) to diagnose a benign mass on unenhanced CT. They showed that chemical shift MRI could characterize four of five adrenal masses with indeterminate CT attenuation (between 1 and 20 H) as benign. However, those four lesions measured 10 H or less on unenhanced CT. The fifth lesion measured between 10 and 20 H but had an adrenal-to-spleen chemical shift ratio greater than 0.7. More important, using an adrenal-to-spleen chemical shift ratio threshold of 0.70 in their study, they correctly identified all malignant lesions.
The optimal threshold to use in diagnosing a lipid-rich adrenal adenoma with chemical shift MRI has yet to be determined. In this study, we used an adrenal-to-spleen chemical shift ratio of less than 0.71 to indicate a lipid-rich adenoma, similar to that used in previous studies [5, 6]. In a study by Mayo-Smith et al. [9], a similar adrenal-to-spleen chemical shift ratio was obtained but a slightly higher threshold of 0.75 was used and all metastases were correctly classified, although five of 28 adenomas were misclassified. In their study, the adrenal-to-spleen chemical shift ratio was compared with the signal-intensity index (using 5% as the threshold), and it was determined that the adrenal-to-spleen chemical shift ratio was a better quantitative test for discriminating adenomas from metastases. Conversely, Fujiyoshi et al. [8] analyzed four different methods of quantitatively evaluating adrenal adenomas and concluded that the signal-intensity index was the most effective method to distinguish adenomas from metastases. However, the thresholds used to make this distinction were not clearly defined in the study.
In general radiology practice, it is common to qualitatively characterize adrenal masses without obtaining signal-intensity measurements. Mayo-Smith et al. [9] compared a qualitative assessment of adrenal masses with the adrenal-to-spleen chemical shift ratio and found no significant difference in lesion characterization. However in our study, the qualitative and quantitative assessments differed in 15 (36%) of 42 adrenal masses. Although the technique used in the study by Mayo-Smith et al. (which used a 5-point scale of certainty) was slightly different from that used in our study, the reason for the discrepancy is unclear. Nevertheless, the results of this study suggest that qualitative analysis may be less sensitive than quantitative analysis when characterizing adrenal masses on MRI, and it may therefore be prudent to obtain quantitative measurements.
Our study design did not include malignant lesions. In a patient who has a primary neoplasm and an adrenal mass, the proper characterization of the adrenal mass is critical. The diagnosis of an adenoma should be made with very high specificity to avoid misclassification of a metastasis as a benign lesion and should result in fewer adrenal biopsies. Unenhanced CT has been shown to be useful in differentiating lipid-rich adrenal adenomas from other adrenal masses because lipid-rich adenomas have lower CT attenuation values [7]. However, lipid-poor adenomas cannot be differentiated from metastases on unenhanced CT, and in these cases, the identification of negative pixels in the adrenal mass during the portal venous phase of enhancement or delayed CT enhancement washout calculations has proven helpful [10–12]. Although an adrenal washout study is noninvasive, it has risks. When appropriate screening methods are used, iodinated IV contrast material is safe but is still potentially toxic. Furthermore, an adrenal washout study requires additional radiation exposure.
MRI has been shown to be useful and is widely accepted in differentiating
lipid-rich adrenal adenomas from nonadenomas
[4]. In this study, eight (62%)
of 13 indeterminate adrenal masses on unenhanced CT (> 10 H) were
characterized as lipid-rich adenomas using adrenal-to-spleen chemical shift
ratios and signal-intensity indexes. This outcome has important implications
in the algorithm for evaluating an adrenal mass in a patient with cancer. If
an adrenal mass is incidentally found on unenhanced CT and does not meet the
criteria of an adenoma (
10 H), chemical shift MRI could be performed next
for possible characterization, before performing a CT adrenal washout study.
The upper limit of unenhanced CT attenuation of an adrenal mass in which
chemical shift MRI is capable of characterizing a lipid-rich adenoma is not
known. However, in this study, a lipid-rich adrenal adenoma on MRI measured as
high as 26 H on unenhanced CT.
This study has limitations, including its retrospective nature and a case-selection bias for adrenal adenomas. Also, the imaging protocols were not standardized across all cases. This discrepancy may account for some differences between the two techniques. Also, in some cases, the TE was as high as 5.3; therefore, these images may not have been acquired optimally inphase. In addition, some adrenal masses in this series were small (8 mm), and characterizing these masses can be problematic because of partial volume artifacts. This problem is found especially with opposed-phase chemical shift imaging, in which it may be difficult to differentiate loss of signal in the lesion from the India ink artifact surrounding the lesion. In addition, one 4-mm adrenal mass seen on CT was excluded from the cohort because it could not be identified on MRI. Perhaps CT may be a better technique to use when characterizing very small adrenal masses.
Next, in some cases, the interval between CT and MRI was as great as 7 years, and the nature of the lesion could change during the interval. Also, because malignant lesions were not included in this study, it is not possible to determine if an adrenal malignancy could be mistakenly diagnosed as a benign lesion.
Finally, pathologic proof was available for only a single lesion. However, the remaining lesions were characterized using clinically accepted and widely used CT and MRI techniques combined with imaging follow-up. The appropriate length of follow-up to determine that an adrenal mass is benign is not known. In some cases in this series, follow-up imaging was performed for only 6 months. However, this interval has been used by others to show the stability of an adrenal mass over time [11]. Furthermore, the growth of a lesion over time does not necessarily indicate malignancy because even benign adrenal adenomas grow.
In conclusion, incidental adrenal masses are common, and their proper characterization, especially in patients with cancer, is important. In clinical practice, unenhanced CT and chemical shift MRI are both used to differentiate lipid-rich adrenal adenomas from other adrenal masses. However, this study has shown that 62% of adenomas with unenhanced CT attenuation of greater than 10 H can be characterized as lipid-rich using quantitative chemical shift MRI.
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