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1 All authors: Department of Radiology, Osaka University Graduate School of Medicine, 2-2 Yamadaoka, Suita, Osaka 5650871 Japan.
Received August 19, 2002;
accepted after revision May 14, 2003.
Address correspondence to T. Murakami.
Abstract
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MATERIALS AND METHODS. SPIO-enhanced MRI was performed using a 1.5-T system in 33 consecutive patients without cirrhosis who had 81 focal hepatic lesions (42 cysts, 13 hemangiomas, 26 metastatic tumors). The relative signal intensity of lesions on SPIO-enhanced heavily T1- and T2-weighted gradient-echo images was classified into one of the following three categories: high intensity, isointensity, or low intensity relative to the surrounding liver parenchyma. The diagnostic accuracy for differentiating solid metastatic tumors from nonsolid benign lesions (cysts or hemangiomas) was determined.
RESULTS. A combination of the relative signal intensity of the lesion on T2- and heavily T1-weighted gradient-echo images could be classified into the following five categories: high intensity and high intensity (category 1), high intensity and isointensity (category 2), high intensity and low intensity (category 3), isointensity and isointensity (category 4), and isointensity and low intensity (category 5). According to these categories, category 1 contained two hemangiomas, category 2 had 11 hemangiomas, category 3 had 25 metastatic tumors and two cysts, category 4 had three cysts, and category 5 had 37 cysts and one metastatic tumor. When a tumor with a relative signal intensity of categories 1 or 2 was considered to be a hemangioma (category 3 metastatic tumors and categories 4 and 5 cysts), diagnostic accuracy for characterizing such hepatic lesions was 96% (78/81).
CONCLUSION. When evaluating metastatic liver tumors on SPIO-enhanced MRI, we recommend that heavily T1- and T2-weighted gradient-echo images be obtained with our parameters to exclude hemangiomas or cysts.
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Superparamagnetic iron oxide (SPIO) was developed to improve the detectability of hepatic tumors without Kupffer's cells. For this type of imaging, T2-weighted sequences are usually used because SPIO shortens the T2 value of liver parenchyma [2–11]. SPIO also provides new possibilities for characterization of the lesion based on its cellular composition and function rather than on its vascularity and diffusion within the extracellular space [12]. However, when evaluating metastatic liver tumors, it is sometimes difficult to differentiate solid metastatic tumors from nonsolid benign lesions such as hemangiomas or cysts because each lesion shows high intensity on T2-weighted images and SPIO cannot show the hemodynamics of each lesion.
Recently, heavily T1-weighted gradient-echo images with SPIO obtained during a breath-hold have been reported to be useful in detecting metastatic liver tumors because SPIO shortens the T1 value of liver parenchyma, but not of tumors without Kupffer's cells [13, 14]. A combination of T1- and T2-weighted gradient-echo images can be expected to show different signal intensity patterns relative to the liver parenchyma in each kind of solid and nonsolid lesion because the T1 and T2 values for solid and nonsolid lesions are different and SPIO enhances hemangiomas on T1-weighted images as a blood pool agent [15–17].
The purpose of this study was to evaluate the ability of SPIO-enhanced MRI to differentiate solid metastatic tumors from nonsolid benign lesions by clarifying characteristic signal-intensity patterns of each tumor on SPIO-enhanced T2-weighted and heavily T1-weighted gradient-echo images.
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The maximal dimension of the lesions ranged from 5 to 35 mm (mean, 10 mm) for cysts, from 8 to 60 mm (mean, 24 mm) for hemangiomas, and from 8 to 35 mm for metastases (mean, 19 mm). Two hemangiomas in two patients were histologically confirmed by surgical resection. All 42 of the cysts and the 11 hemangiomas were confirmed on the basis of a combination of clinical and radiologic criteria consisting of tumor markers and dynamic MRI and CT examinations. Five metastatic tumors in four patients were histologically confirmed by surgical resection. The other metastatic lesions were confirmed by using a combination of clinical and radiologic criteria, including response to transcatheter arterial chemotherapy or progression or regression in size. In addition, patients underwent follow-up CT and MRI more than 6 months later. The metastases originated from the following primary tumors: colon carcinoma (n = 16), breast carcinoma (n = 5), mesenteric leiomyosarcoma (n = 3), gastric carcinoma (n = 1), and cervical carcinoma (n = 1). Any lesion detected on MRI alone was excluded from this study because we could not confirm the lesion by our imaging criteria mentioned previously.
Ferumoxides (Feridex, Eiken and Tanabe Pharmaceutical, Osaka, Japan), a SPIO preparation coated with low-molecular-weight dextran, was used. The physical, pharmacokinetic, and biologic properties of the SPIO have been reported previously [19]. This agent was supplied in 5-mL vials containing 11.2 mg of iron and 61.3 mg of mannitol per milliliter. A dose of 0.56 mg (10 µmol) of iron per kilogram of body weight was diluted with 100 mL of 5% dextrose solution and infused IV at a rate of 3 mL/min through an in-line 5-µm filter.
MRI was performed on either a Signa Horizon LX 1.5-T system (General Electric Medical Systems, Milwaukee, WI) (23 patients) or a Magnetom Vision 1.5-T system (Siemens, Erlangen, Germany) (10 patients). For all cases, phased array coils (Torso-array coil, General Electric Medical Systems; or CP body array coil, Siemens) were used for reception of the signal. All MRIs were obtained in the axial plane.
Approximately 60 min after the initiation of IV drip infusion of the SPIO for 30 min, heavily T1- and T2-weighted fast low-angle shot or fast spoiled gradient-echo with steady-state images were obtained. A TR of 150, TE range of 1.3–2.2, and a flip angle of 90° were used for heavily T1-weighted gradient-echo images, and a TR of 150, a TE range of 10–12, and flip angle of 60° were used for T2-weighted gradient-echo images. All images were obtained during a 17-sec breath-hold in the axial plane with a section thickness of 8 mm, an interslice gap of 2 mm, a matrix size of 130 x 256, a field of view of 280 x 320 mm, and 1 excitation. A TR of 150 was used to maximize anatomic coverage within the time frame of a reasonable breath-hold. Breath-held images were obtained at end-expiration in all cases. No presaturation pulses were used in order to eliminate the increase in the requisite breath-hold times. Respiratory-triggered T2-weighted fast spin-echo sequences with a TR range of 3,750–8,000 (mean, 4,974), effective TE range of 65–80, echo-train length of 8, 3 signals acquired, and a matrix size of 512 x 160 were also obtained.
In this study, the signal intensity of the lesion relative to that of the surrounding liver parenchyma only on ferumoxides-enhanced MRI with the two sequences (heavily T1- and T2-weighted gradient-echo images) was evaluated qualitatively by two radiologists in consensus who were experienced in liver imaging. During the analysis, no other sequences were available. The two observers knew of the presence and location of liver lesions but were unaware of other imaging findings and the patients' diagnoses. The relative signal intensity of the lesions was classified into the following three categories: high intensity relative to the surrounding liver parenchyma, isointensity, and low intensity. Only in the lesions over which there was disagreement between the two radiologists, even after discussion, were MRI values of region of interest (circle, 5 mm in diameter) of both the lesion and the surrounding liver parenchyma measured for reference. After blinded reviewing, the signal intensity of each lesion was also observed on T2-weighted fast spin-echo images, retrospectively.
The diagnostic accuracy for differentiating solid metastatic tumors from nonsolid benign lesions (cysts or hemangiomas) using the characteristic signal-intensity pattern of each lesion on the two sequences was determined.
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Of the 42 cysts, 40 lesions showed isointensity on the T2-weighted gradient-echo images (Fig. 1A). Of these 40 lesions, 37 showed low intensity (Fig. 1B) whereas the remaining three lesions showed isointensity on the heavily T1-weighted gradient-echo images. The three lesions were less than 5 mm in diameter. The remaining two of the 42 cysts revealed high intensity on the T2-weighted gradient-echo images and low intensity on the heavily T1-weighted gradient-echo images (Fig. 2A, 2B). The two lesions were 35 mm and 18 mm in diameter and were larger than the other cysts.
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All 13 hemangiomas showed high intensity on the T2-weighted gradient-echo images (Fig. 3A). Eleven of the 13 lesions showed isointensity (Fig. 3B), and the other two showed high intensity on the heavily T1-weighted gradient-echo images.
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Of the 26 metastatic lesions, 25 showed high intensity (Fig. 4A) on the T2-weighted gradient-echo images. All 25 lesions showed low intensity on the heavily T1-weighted gradient-echo images (Fig. 4B). Another lesion, which was less than 10 mm in diameter in the subphrenic location of segment VIII and originating from mesenteric leiomyosarcoma, showed isointensity on the T2-weighted gradient-echo images. This lesion showed low intensity on the heavily T1-weighted gradient-echo images (Fig. 5A, 5B). All 26 lesions revealed low intensity on the heavily T1-weighted gradient-echo images.
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A combination of the relative signal intensity of the lesion on each sequence could be classified into the following five categories: high-intensity heavily T1-weighted gradient-echo images and high-intensity T2-weighted gradient-echo images (category 1), isointense heavily T1-weighted gradient-echo images and high-intensity T2-weighted gradient-echo images (category 2), low-intensity heavily T1-weighted gradient-echo images and high-intensity T2-weighted gradient-echo images (category 3), isointense heavily T1-weighted gradient-echo images and isointense T2-weighted gradient-echo images (category 4), low-intensity heavily T1-weighted gradient-echo images and isointense T2-weighted gradient-echo images (category 5).
According to this classification, category 1 contained two hemangiomas, category 2 had 11 hemangiomas, category 3 had 25 metastatic tumors and two cysts, category 4 had three cysts, and category 5 had 37 cysts and one metastatic tumor. When a tumor with a relative signal intensity of category 1 or 2 was considered to be a hemangioma (category 3 metastatic tumors and category 4 or 5 cysts), diagnostic accuracy for characterizing such hepatic lesions was 96% (78/81).
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To our knowledge, the efficacy of characterization of hepatic tumors by SPIO-enhanced MRI combined with the most recently optimized sequences, such as various gradient-recalled echo sequences, has not been evaluated in previous comparative studies. In this study, we used gradient-echo sequences with long TEs (T2-weighted gradient-echo images). In this sequence, T2 relaxations are strongly affected by local field inhomogeneities (intravoxel dephasing). SPIO can have a large longitudinal relaxivity value, which can reduce the T1 value more than gadopentetate dimeglumine. Therefore, we also used heavily T1-weighted gradient-echo images obtained during breath-hold because this sequence was reported to be useful in detecting metastatic liver tumors because SPIO shortens the T1 value of liver parenchyma but not that of lesions without Kupffer's cells. Each kind of solid and nonsolid lesion can be expected to show different signal-intensity patterns relative to the liver parenchyma on T1- and T2-weighted gradient-echo images because T1 and T2 values of solid or nonsolid lesions are different and SPIO enhances hemangiomas on T1-weighted gradient-echo images as a blood pool agent [15–17].
Forty of 42 cysts showed isointensity on T2-weighted gradient-echo images. Because the T2-weighted gradient-echo images in this study used a relatively large flip angle of 60°, T1 contrast of cysts with long T1 values suppressed T2 contrast. The two cysts that showed high intensity on T2-weighted gradient-echo images were relatively larger than the other cysts. We believe that the T2 value of large cysts with a large amount of serous fluid and without partial volume effect was longer than small cysts. This signal pattern was considered to be indicative of metastasis according to our category. In this study, blinded reviewers did not assess T2-weighted fast spin-echo images at the time of blinded reviewing, but we can speculate that T2-weighted single-shot fast spin-echo imaging may be helpful because large serous cysts usually show markedly higher intensity, although this evaluation was not an objective of our analysis. On the heavily T1-weighted gradient-echo images, 37 cysts showed low intensity relative to the liver parenchyma enhanced by SPIO, but three cysts showed isointensity. We speculated that the reason was that these small cysts showed increased signal because of a partial volume effect.
Hemangiomas showed iso- or high intensity on the heavily T1-weighted gradient-echo images with short TEs. Hemangiomas were reported to be enhanced by SPIO on T1-weighted gradient-echo images [15–17] because SPIO is not only taken up by the macrophages and endothelial cells of hemangiomas but also accumulates in a blood pool of hemangioma because of the prolonged circulation of the contrast agent. All 13 hemangiomas showed high intensity on T2-weighted gradient-echo images with long TEs. The reason for this was thought to be because both T1 values shortening of the lesion due to SPIO and originally long T2 values of the lesion reflected the high signal intensity of hemangiomas on the T2-weighted gradient-echo images with relatively large flip angles and long TE sequences.
Twenty-five of 26 metastatic tumors showed high intensity, but the other one showed isointensity on T2-weighted gradient-echo images. This lesion was less than 10 mm in diameter. We thought that this small lesion could not be detected because of a partial volume effect. On unenhanced T2-weighted fast or single-shot fast spin-echo images, cysts and hemangiomas may show a higher signal intensity than metastatic tumors. Therefore, as mentioned previously, SPIO-enhanced T2-weighted single-shot fast spin-echo imaging may also provide us with useful information for the differential diagnosis of hepatic lesions, although this possibility is just speculation.
The T2-weighted gradient-echo images used in this study might be reflected by both T1 and T2 values because a large flip angle of 60° and a long TE of 10 were used. We used a large flip angle to increase the signal-to-noise ratio of the images and a long TE to emphasize signal loss due to the susceptibility effect of SPIO. We called the sequence T2-weighted gradient-echo images in this study because we think this sequence largely reflects the T2 value (susceptibility) on SPIO-enhanced MRI.
This study evaluated only contrast-enhanced images because a long time is required for obtaining both unenhanced and SPIO-enhanced MRI. However, our data show that contrast-enhanced images are sufficient for differentiating hepatic lesions.
Our study did not include patients with cirrhosis and hepatocellular carcinomas because tumor contrast relative to the liver parenchyma may change due to Kupffer's cell function, which is one kind of hepatic function. Hepatocellular carcinomas show variable signal intensity relative to the liver parenchyma on T1-weighted gradient-echo images with short TEs. Moreover, some hepatocellular carcinomas, especially well-differentiated tumor grades, have a certain number of Kupffer's cells and may uptake SPIO [12]. This uptake function by Kupffer's cells may be decreased in cirrhotic livers. Therefore, it is difficult to diagnose tumors of hepatocellular origin by comparing the signal intensity of the tumor with that of liver parenchyma on SPIO-enhanced MRI. However, patients with metastatic tumors, cysts, or hemangiomas in this study had normal liver function. SPIO was developed largely for improving detection of metastatic hepatic lesions, and we therefore believe that the fact that this study included no patients with hepatocellular carcinoma is not a shortcoming.
In this study, metastatic lesions were mostly derived from colon cancer. Many kinds of metastatic tumors have different T1 or T2 values. Some of them might not be included in the diagnostic criteria used by this study. Further studies are needed.
In this study, previously obtained images were reviewed by the two observers. However, only the study designer and coordinator knew how the patients were selected, and although the two observers knew of the presence and location of the liver lesions, they were unaware of other imaging findings and their corresponding diagnoses. We therefore believe there was no bias at the time of the reviewing.
Another criticism of our study could be the lack of histologic proof for each lesion. However, all lesions had several confirmatory studies, such as sonography, enhanced CT, enhanced MRI, and follow-up imaging studies. Moreover, we could follow up the course of some lesions over time and in response to therapy, especially transcatheter arterial chemotherapy.
The results of this study show potential in determining specific diagnoses of metastatic tumors by using SPIO-enhanced heavily T1- and T2-weighted gradient-echo images. We recommend that when evaluating metastatic liver tumors on SPIO-enhanced MRI, heavily T1- and T2-weighted gradient-echo images be obtained with our parameters to exclude hemangiomas or cysts.
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