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DOI:10.2214/AJR.07.2467
AJR 2008; 191:285-289
© American Roentgen Ray Society

Clinical Observations

Chemoembolization of Hepatic Metastases from Ocular Melanoma: Assessment of Response with Contrast-Enhanced and Diffusion-Weighted MRI

Manon Buijs1, Josephina A. Vossen, Kelvin Hong, Christos S. Georgiades, Jean-Francois H. Geschwind and Ihab R. Kamel

1 All authors: Russell H. Morgan Department of Radiology and Radiological Sciences, Johns Hopkins Hospital, 601 N Caroline St., Rm. 3235A, Baltimore, MD 21287.

Received April 25, 2007; accepted after revision January 6, 2008.

 
M. Buijs and J. A. Vossen contributed equally to the manuscript.

Address correspondence to I. R. Kamel (ikamel{at}jhmi.edu).


Abstract
Top
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 References
 
OBJECTIVE. The purpose of this study was to assess the utility of assessment of tumor size and enhancement with diffusion-weighted and conventional MRI in the evaluation of response to transarterial chemoembolization therapy for metastatic ocular melanoma.

CONCLUSION. In patients with ocular melanoma and liver metastasis treated with transarterial chemoembolization, functional MRI showed significant changes in the lesions. These changes included a decrease in tumor enhancement and an increase in the apparent diffusion coefficient of the tumor, suggesting increasing tumor necrosis and cell death.

Keywords: diffusion-weighted MRI • hepatic metastases • liver • metastatic ocular melanoma • perfusion MRI • transarterial chemoembolization • treatment response


Introduction
Top
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 References
 
Ocular melanoma arising from melanocytes in the uvea (uveal melanoma) is the most common primary malignant tumor of the eye. The incidence in the United States is 4.3 cases per million persons per year. Uveal melanoma constitutes 85–95% of ocular melanomas. The reported 5-year survival rate for ocular melanoma ranges from 31% to 80% [1, 2]. The liver is the most common site of metastatic disease, with liver metastasis occurring in as many as 50% of patients [3, 4]. The prognosis of metastatic ocular melanoma is poor with median survival periods of 2 months without treatment and 5–9 months with treatment [5, 6].

Various treatment techniques exist for patients with metastatic ocular melanoma, including surgical resection, systemic chemotherapy, and locoregional therapy [7, 8]. Monitoring the effectiveness of transarterial chemoembolization (TACE), a locoregional therapy, with imaging is important in determining treatment success and in guiding future therapy. However, imaging techniques and imaging response criteria have been limited in giving clinically satisfactory information about the extent of tumor necrosis.

The apparent diffusion coefficient (ADC) calculated in diffusion-weighted MRI has become a promising biomarker of tumor response to therapy [9]. The ADC is a measure of the mobility of water in tissues. Viable tumors are high in cellularity, and the cells have an intact cell membrane that restricts the mobility of water molecules and results in a relatively low ADC. Conversely, cellular necrosis increases membrane permeability, allowing water molecules to move freely and causing a relative increase in ADC. Diffusion-weighted MRI has been used to assess tumor response after chemotherapy and radiation therapy.

The primary application of diffusion-weighted MRI has been in brain imaging [10–12]. In the liver, diffusion-weighted imaging has been used to characterize focal hepatic lesions and to assess tumor response to locoregional therapy [13, 14]. We hypothesize that diffusion-weighted MRI can be added to contrast-enhanced MRI to determine the presence of cellular necrosis and therefore be useful in obtaining information about tumor response to TACE. To our knowledge, the use of diffusion-weighted imaging in the follow-up of metastatic ocular melanoma has not been described. The purpose of our study was to assess the value of diffusion-weighted MRI in the evaluation of tumor response to TACE for metastatic ocular melanoma.


Materials and Methods
Top
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 References
 
Patients
This study was a retrospective analysis of a prospectively collected database. The study population consisted of six patients with metastatic ocular melanoma who underwent TACE. The criterion for TACE was confirmed diagnosis of unresectable metastatic ocular melanoma in pa tients with or without minimally impaired liver function. Patients excluded from TACE were those with Eastern Cooperative Oncology Group per formance status greater than grade 2, encephal opathy, severe variceal bleeding or severe ascites, clinically significant thrombocytopenia (platelet count < 50,000/mL), impaired renal function (creatinine concentration > 2 mg/dL), or severe liver failure (advanced Child-Pugh class C or serum bilirubin concentration > 2 mg/dL). The study group included all patients treated with chemoembolization who underwent contrast-enhanced and diffusion-weighted MRI before and after treatment. Between January 1, 2003, and December 31, 2006, the care of eight patients with metastatic ocular melanoma who underwent one or more cycles of TACE was discussed by the liver tumor board at our institution, and six of the patients fulfilled the inclusion criteria. The other two patients did not undergo MRI after TACE and were excluded. The diagnosis of metastatic ocular melanoma was confirmed by biopsy of liver meta static lesions in all patients. Data were col lected prospectively, and the study was authorized by the institutional review board.

Chemoembolization Technique
All chemoembolization procedures were performed by one experienced interventional radiologist using the same technique in all pro cedures. A 5.0-French micropuncture intro ducer set was used to access the right common femoral artery with the Seldinger technique. After a 0.035-inch Bentson guidewire was advanced into the abdo minal aorta, the needle was exchanged for a 5-French vascular sheath, which was placed into the right common femoral artery under fluoro scopic guidance. Through the sheath, a 5-French catheter (Glidecath Simmons-1, Terumo) was advanced into the aorta and reformed in the aortic arch. Selective angiography of the celiac axis was performed. The catheter was advanced into the hepatic artery branch indicated by the tumor location. If selective catheterization was necessary, a 3-French catheter (Renegade Hi-Flow, Boston Scientific) was used.

Once the appropriate catheter (5-French Sim mons 1, 3-French microcatheter, or other selected catheter) was in position, TACE was performed through the catheter to achieve lobar or segmental embolization according to the target lesions. A solution containing 100 mg of cisplatin (Platinol, Bristol-Myers Squibb), 50 mg of doxorubicin (Adriamycin, Pharmacia-Upjohn), and 10 mg of mitomycin C (Mutamycin C, Bedford Laboratories) in a 1:1 mixture with iodized oil followed by infusion of 300- to 500-µm embolic microspheres (Embo sphere, Biosphere Medical) was admin istered until stasis was achieved.

CT Technique
Within 1 day after chemoembolization, all patients underwent unenhanced helical CT (Sens ation 16 scanner, Siemens Medical Solu tions). The scanning parameters were 120 kVp, 210 mA, 5-mm section collimation, and 5-mm image reconstruction. Technical success of the procedure was confirmed with focal deposition of iodized oil in the targeted segment or lobe of the liver.

MRI Technique
A 1.5-T MRI unit (CV/i, GE Healthcare) and phased-array torso coil were used. The imaging protocol consisted of T2-weighted fast spin-echo images (TR/TE, 5,000/100; matrix size, 256 x 256; slice thickness, 8 mm; interslice gap, 2 mm; receiver bandwidth, 32 kHz), breath-hold diffusion-weighted echo-planar images (5,000–6,500/110; matrix size, 128 x 128; slice thickness, 8 mm; interslice gap, 2 mm; b value, 500; receiver bandwidth, 32 kHz) along the section-select gradient (z-axis), and breath-hold unenhanced and contrast-enhanced (0.1 mmol/kg IV gadodiamide, Omniscan, GE Healthcare) T1-weighted 3D fat-suppressed spoiled gradient-echo images (5.1/1.2; field of view, 320–400 mm; matrix size, 192 x 160; slice thickness, 4–6 mm; receiver bandwidth, 64 kHz; flip angle, 15°) in the arterial phase (20 seconds) and portal venous phase (60 seconds). Typical acquisition time was a single breath-hold of 30 seconds to cover the entire liver.

Follow-Up
According to protocol, patients underwent contrast-enhanced and diffusion-weighted MRI 4–6 weeks after TACE for assessment of tumor response. Patients with near complete tumor necrosis determined by lack of enhancement on MRI and an increase in ADC of the lesion did not undergo additional treatments and underwent follow-up imaging every 6–8 weeks. Patients with residual enhancement whose clinical perform ance status was maintained underwent additional TACE treatments.

Image Analysis
MR image processing and ADC maps were generated with a commercially available workstation (Advantage Windows, GE Health care). Images were interpreted by consensus of two experienced MRI radiologists in the same session. Parameters evaluated included change in tumor size, enhancement, and ADC. For patients who under went more than one TACE cycle, the MR images obtained after the last cycle were used for comparison.

All target lesions 2 cm or larger in the treated lobe were evaluated; a maximum of four lesions per patient were used to ensure independent sampling. The target lesions were selected by consensus of two radiologists. Target lesions in the treated lobe of the liver were selected. The maximum diameter of the targeted lesions was measured with electronic calipers as proposed in the Response Evaluation Criteria in Solid Tumors (RECIST). Areas of tumor enhancement were considered viable, and areas without enhancement were considered necrotic, as suggested by the European Association for the Study of the Liver [15]. Percentage enhancement was based on enhancement seen on the axial arterial and portal venous phase MR images with the largest tumor size. Complete absence of enhancement was reported as 0%. Enhancement was reported as 25% if there was 25% or less enhancement, 50% if more than 25% and up to 50% enhancement, 75% if more than 50% and up to 75% enhancement, and 100% if greater than 75% enhancement was present.

In cases of lesions that had higher signal intensity than the surrounding liver parenchyma on unenhanced T1-weighted images, subtraction was performed to assess for enhancement. ADC maps were generated from the diffusion-weighted images side by side with the gadolinium-enhanced images, and mean values were recorded by placement of a region of interest (ROI) over the entire treated mass seen on the image with the largest lesion size. ROIs placed on the diffusion-weighted images were automatically generated in the same location on the images with ADC maps. ADC maps of normal-appearing liver, spleen, and par aspinal muscle were generated. Percentage iodized oil deposition on CT was recorded and reported as 25% if 25% or less of the tumor exhibited iodized oil uptake, 50% if more than 25% and up to 50% of the tumor exhibited uptake, 75% if more than 50% and up to 75% of the tumor exhibited uptake, and 100% if 75% or more of the tumor exhibited uptake. For patients who had undergone multiple iodized oil treatments, the mean maximum iodized oil retention in the targeted lesion was recorded.

Statistical Analysis
Statistical analysis was performed with the Stata software package (version 8, Stata). A paired Student's t test was used to compare tumor sizes, degrees of enhancement, and ADCs before and after TACE to evaluate tumor response. A paired Student's t test also was used to compare ADCs of liver, spleen, and muscle before and after treatment. A value of p < 0.05 was considered to indicate statistical significance.


Results
Top
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 References
 
Demographic Information and Tumor Features
A total of 21 lesions were evaluated in six patients (two men, four women; mean age, 70 years). All lesions were located in the right lobe of the liver. Eleven lesions received a single TACE treatment, seven lesions received two cycles of TACE, and three lesions received three cycles of TACE. The average duration between preprocedural and postprocedural MRI was 79 days (range, 32–161 days). MRI was performed within 16 days (range, 1–45 days) before TACE. The mean interval between the last TACE treatment and follow-up MRI was 33 days (range, 21–45 days). On T1-weighted MRI before TACE, 17 lesions were hypointense, three lesions were isointense, and one lesion was hyperintense compared with the surrounding liver parenchyma. After TACE, 15 lesions were hypointense, one lesion was isointense, and six lesions were hyperintense on T1-weighted MRI. On T2-weighted MRI before treatment, 19 lesions were hyperintense and two lesions were isointense compared with the surrounding liver parenchyma. After TACE, 20 lesions were hyperintense and one lesion was isointense on T2-weighted MRI. Mean iodized oil retention within the tumor on CT was 45%.


Figure 1
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  		Fig. 1A —60-year-old woman with hepatic metastases from ocular melanoma. Changes in enhancement and apparent diffusion coefficient after transarterial chemoembolization. Gadolinium-enhanced arterial phase MR image (TR/TE, 5.1/1.2) shows 3.1-cm mass (arrow) in left lobe with almost complete (100%) enhancement.

 


Figure 2
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  		Fig. 1B —60-year-old woman with hepatic metastases from ocular melanoma. Changes in enhancement and apparent diffusion coefficient after transarterial chemoembolization. Diffusion-weighted MR image (6,500/110) shows hyperintense mass (arrow).

 


Figure 3
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  		Fig. 1C —60-year-old woman with hepatic metastases from ocular melanoma. Changes in enhancement and apparent diffusion coefficient after transarterial chemoembolization. After placement of region of interest on entire mass (arrow), apparent diffusion coefficient is 0.00138 mm2/s.

 
Assessment of Change in MRI Parameters After TACE
On gadolinium-enhanced MRI, overall tumor enhancement on a lesion-by-lesion basis in the arterial and portal venous phases decreased significantly after TACE (Table 1). Arterial phase enhancement decreased 41% after TACE, and the decrease was statistically significant (p = 0.0002). Venous phase enhancement decreased 56%, also statistically significant (p < 0.0001). Diffusion-weighted MRI was useful in monitoring response after treatment. The mean tumor ADC increased 48% after TACE (p = 0.0003), whereas the ADC re mained unchanged in nontumorous liver, spleen, and muscle (Fig. 1A, 1B, 1C, 1D, 1E, 1F, 1G, Table 1). Figure 2 shows changes in ADC after treatment. Although mean tumor size decreased 16% from 4.9 to 4.1 cm after TACE, none of the lesions met the RECIST for complete response (disappearance of all measurable disease), and only eight lesions were considered partial responders (> 30% decrease in size).


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  		TABLE 1: Mean Changes in Tumor Size, Enhancement, and ADC Value After TACE

 

Figure 4
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  		Fig. 1D —60-year-old woman with hepatic metastases from ocular melanoma. Changes in enhancement and apparent diffusion coefficient after transarterial chemoembolization. Unenhanced CT scan of abdomen shows intense deposition of iodized oil in mass (arrow) after transarterial chemoembolization.

 

Figure 5
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  		Fig. 1E —60-year-old woman with hepatic metastases from ocular melanoma. Changes in enhancement and apparent diffusion coefficient after transarterial chemoembolization. Gadolinium-enhanced arterial phase MR image (TR/TE, 5.1/1.2) after transarterial chemoembolization shows significant decrease in enhancement of mass (arrow), now less than 10%. Size of mass decreased slightly to 2.9 cm.

 

Figure 6
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  		Fig. 1F —60-year-old woman with hepatic metastases from ocular melanoma. Changes in enhancement and apparent diffusion coefficient after transarterial chemoembolization. Diffusion-weighted MR image (6,500/110) after transarterial chemoembolization.

 

Figure 7
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  		Fig. 1G —60-year-old woman with hepatic metastases from ocular melanoma. Changes in enhancement and apparent diffusion coefficient after transarterial chemoembolization. After placement of region of interest on entire mass (arrow), apparent diffusion coefficient is 0.00229 mm2/s, confirming increasing cellular necrosis.

 

Figure 8
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  		Fig. 2 —Graph shows changes in apparent diffusion coefficient after treatment. ADC = apparent diffusion coefficient.

 


Discussion
Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
References
 
The overall prognosis among patients with primary ocular melanoma is good. However, liver metastasis develops in 40–50% of the patients and is related to a poor median survival time of 2–9 months [5, 6]. Among these patients TACE can result in clinically significant regression of hepatic metastasis and lengthen overall survival [7]. In this setting it is critical to assess tumor response. Studies have shown that diffusion-weighted MRI can be used to identify and characterize hepatic lesions and assess tumor response after locoregional therapy [16]. The objective of our study was to use the criteria of iodized oil deposition, tumor size, and tumor enhancement to assess the utility of diffusion-weighted and conventional MRI in the evaluation of tumor response after TACE for metastatic ocular melanoma. Our results indicate that diffusion-weighted and contrast-enhanced MRI can be used to detect tumor necrosis before reduction in tumor size occurs.

Several imaging techniques are used in traditional assessment of tumor response. One of the RECIST is change in tumor size on CT or MRI. Patients who have complete disappearance of all disease are considered responders. Partial response requires a greater than 30% decrease in tumor size. After TACE, however, many lesions do not initially decrease in size. To address this issue, the European Association for the Study of the Liver has officially recommended the use of lesion enhancement on contrast-enhanced CT as the standard factor for determining treatment response after locoregional therapy [15]. Enhanced portions of the tumor are presumed to be viable, whereas unenhanced portions are presumed necrotic. However, accumulation of iodized oil after TACE limits the use of enhancement on contrast-enhanced CT. At our institution we therefore use contrast-enhanced MRI to evaluate enhancement after TACE.

Our data showed that none of the treated lesions was considered a complete responder on the basis of RECIST. Therefore, our results suggest that the RECIST are not useful in determining early tumor response after TACE. Contrast-enhanced MRI depicts areas of tumor enhancement with extracellular contrast agents. Hepatic metastatic lesions of ocular melanoma, however, are already hyperintense on T1-weighted images, and this factor may interfere with accurate determination of contrast enhancement on nonsubtracted images. In this study we saw a significant decrease in enhancement after TACE, indicating that tumor enhancement can be used as a predictor of tumor response.

The mobility of water molecules in tissues is represented by the ADC on diffusion-weighted MRI. This value provides insight into tumor microstructure. Viable tumors contain cells with an intact cell membrane that restricts water mobility and causes low ADCs. Conversely, cellular necrosis increases membrane permeability, which increases the ADC. These characteristics are used to detect cellular necrosis before size regression occurs [17]. Our study showed a significant increase in ADCs of the lesions after treatment, indicating marked cellular necrosis in response to therapy. The ADCs of normal liver tissue, spleen, and muscle showed no significant changes after treatment.

This study had several limitations. First, the patient population was relatively small, so further studies with a larger sample size are needed to confirm our conclusions and to stratify patients into responders and nonresponders. The objective would be to establish a cutoff value between the two groups. A second limitation was possible selection bias, because only patients who underwent MRI before and after treatment were included in the study. Another limitation was the lack of histopathologic correlation of the lesions after chemoembolization. For ethical reasons, we did not obtain histologic correlation in this study. In addition, we could not confirm that the changes in ADC were due only to cellular necrosis and not to oil deposition within the tumor. Our results, however, are in line with those of a previous evaluation of the use of diffusion-weighted imaging after 90Y-microsphere treatment without oil deposition [18]. Changes in ADC occurred only in the targeted tumors, whereas the nontargeted tumors in the contralateral lobe of the liver had no change in ADCs. Therefore, we believe that these changes are due to cellular necrosis resulting from the targeted therapy. Last, we did not perform a reproducibility analysis of our imaging sequence because it was not one of the study objectives. However, our results are in line with those of a previous work [19] that showed an increase in ADC values after locoregional therapy.

Our results indicate that diffusion-weighted MRI can be useful for assessing tumor response after TACE in patients with metastatic ocular melanoma.


References
Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 

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