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DOI:10.2214/AJR.07.2675
AJR 2008; 190:99-104
© American Roentgen Ray Society

Original Research

Hepatic Arterial Chemoembolization for Management of Metastatic Melanoma

Karun V. Sharma1, Jennifer E. Gould1,2, J. William Harbour2,3, Gerald P. Linette2,4, Thomas K. Pilgram1, Pouya N. Dayani3 and Daniel B. Brown1,2,5

1 Mallinckrodt Institute of Radiology, Washington University School of Medicine.
2 Siteman Comprehensive Cancer Center, Washington University School of Medicine, St. Louis, MO.
3 Department of Ophthalmology, Washington University School of Medicine, St. Louis, MO.
4 Division of Oncology, Department of Medicine, Washington University School of Medicine, St. Louis, MO.
5 Present address: Division of Cardiovascular and Interventional Radiology, Thomas Jefferson University Hospital, Suite 4200 Gibson Bldg., 111 S 11th St., Philadelphia, PA 19107.

Received June 5, 2007; accepted after revision August 7, 2007.

 
Address correspondence to D. B. Brown.


Abstract
Top
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 References
 
OBJECTIVE. Hepatic arterial chemoembolization is an accepted therapy for stage 4 melanoma with liver-dominant metastasis. However, the reports of outcomes are limited. We present our outcomes with hepatic arterial chemoembolization for metastasis of stage 4 melanoma.

MATERIALS AND METHODS. Twenty patients with liver-dominant metastasis of ocular or cutaneous melanoma were treated with hepatic arterial chemoembolization. Overall survival and progression-free survival rates were calculated from the first treatment. Patients with intrahepatic tumor progression were treated with additional hepatic arterial chemoembolization. Both overall survival and progression-free survival were analyzed with the Kaplan-Meier method. Tumor pattern on angiography was characterized as either nodular or infiltrative on the basis of angiographic appearance.

RESULTS. The 20 patients underwent 46 hepatic arterial chemoembolization sessions (mean, 2.4 sessions; range, 1-5). The mean and median overall survival times were 334 ± 71 and 271 days, respectively. There were no deaths within 30 days of treatment. Thirteen of the 20 patients had progression of disease. The mean and median progression-free survival times for these patients were 231 ± 42 and 185 days, respectively. Patients with lesions that had a nodular angiographic appearance had longer progression-free survival than patients with lesions that had an infiltrative appearance (mean progression-free survival time, 249 vs 63 days). Patients with lesions that had a nodular angiographic appearance also survived significantly longer than those with lesions that had an infiltrative angiographic pattern (mean overall survival time, 621 vs 114 days; p = 0.0002).

CONCLUSION. Hepatic arterial chemoembolization for liver-dominant metastasis of stage 4 melanoma is a safe treatment that results in longer survival than has occurred among historical controls. Patients with lesions that have a nodular tumor appearance on angiography survive significantly longer than patients with lesions that have an infiltrative appearance on angiography.

Keywords: hepatic arterial chemoembolization • liver • metastatic disease • metastasis • ocular melanoma


Introduction
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 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 References
 
The overall incidence of liver-dominant metastatic melanoma is low, particularly in comparison with that of other primary tumors, such as colon and breast cancer. Ocular melanoma is the most common intraocular malignant tumor in adults [1-3]. Despite undergoing apparently definitive management of the primary tumor with either enucleation or plaque radiation therapy, many patients eventually have a relapse, and distant metastatic lesions develop, most commonly in the liver. Once hepatic metastasis occurs, the prognosis is extremely poor; the mean survival period is approximately 4 months despite salvage chemotherapy [3, 4]. Cutaneous melanoma rarely results in liver-dominant metastasis. When this type of metastasis does occur, chemotherapeutic options are limited.

Hepatic arterial chemoembolization for the management of hepatic metastasis of melanoma was first reported in 1988 [2]. Chemoembolization achieves greater drug concentration within the tumor than does systemic chemotherapy while decreasing systemic toxicity such as myelosuppression [5]. A retrospective analysis [6] showed that hepatic arterial chemoembolization with a cisplatin-based regimen was the only technique resulting in improved survival compared with other treatments, including systemic chemotherapy and chemotherapy through a surgically implanted arterial port. However, reports of outcomes remain extremely limited. The primary goal of hepatic arterial chemoembolization is to arrest progression of disease. A common finding in existing studies is that a large number of patients experience disease progression despite treatment with hepatic arterial chemoembolization, the reported response rates being less than 50% [6, 7]. To date there has been no method, to our knowledge, of predicting which patients will respond to therapy. The reported survival times among patients who do respond to treatment range from 14 to 22 months [6, 7]. In this study, we evaluated our institutional experience with a multidrug hepatic arterial chemoembolization regimen of cisplatin, doxorubicin, and mitomycin C in the treatment of patients with liver-dominant metastasis of melanoma. The principle outcome investigated was overall survival in a contemporary cohort. A secondary measure was angiographic findings, which suggest there are two distinct forms of hepatic metastatic disease that respond differently to hepatic arterial chemoembolization and are predictive of outcome.


Figure 1
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  		Fig. 1 —Graph shows results of Kaplan-Meier analysis of overall survival for entire group after hepatic arterial chemoembolization. Calculated mean and median survival times were 334 ± 71 and 272 days, respectively.

 


Figure 2
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  		Fig. 2 —Graph shows results of Kaplan-Meier analysis of time to progression for entire group after hepatic arterial chemoembolization. Calculated mean and median times to progression were 231 ± 42 and 185 days, respectively.

 

Materials and Methods
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 Materials and Methods
Results
 Discussion
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This study was approved by our institutional review board. All patients underwent cross-sectional imaging with contrast-enhanced CT, PET/CT, or both within 1 month before treatment. Informed consent was obtained from all patients. On the day of treatment, laboratory data, including complete blood cell count, complete metabolic panel, and prothrombin time, were obtained. Standard preprocedural medications (8 mg ondansetron, 10 mg dexamethasone, and 500 mg metronidazole) were administered.

Local anesthesia was obtained with 1% buffered lidocaine, and sedation was achieved with IV midazolam and fentanyl. The Seldinger technique was used to access the common femoral artery. Superior mesenteric angiography was performed though the portal venous phase to evaluate for portal vein patency and flow direction and variant arterial anatomic features. Celiac artery angiography was followed by subselection of the right or left hepatic artery with a microcatheter. After confirmation of the appropriate position, chemoembolization was performed with a mixture of 50 mg cisplatin, 50 mg doxorubicin, and 10 mg mitomycin C dissolved in sterile contrast material (ioversol, Optiray 350, Mallinckrodt Medical) and emulsified with ethiodized oil (Ethiodol, Savage Laboratories). After infusion of the chemotherapeutic agents under fluoroscopic monitoring, embolization was performed with either absorbable gelatin sponge (Gelfoam, Upjohn) slurry or 300-500 µm polyvinyl alcohol (PVA) particles mixed in contrast material until near stasis of flow in tumor-feeding branches was achieved. Use of PVA was reserved for cases in which feeding arteries were severely pruned from previous treatment. The decision to use PVA was made by the primary operator at the time of the procedure. Use of PVA did not limit further hepatic arterial chemoembolization. Aliquots of 1-3-mL of 1% lidocaine were intermittently administered intraarterially during infusion of the chemotherapeutic mixture [8]. Up to one lobe was treated per hepatic arterial chemoembolization session; the contralateral lobe was treated 4-6 weeks after the first procedure.

After the procedure, patients received maintenance IV antiemetics and antibiotics (8 mg ondansetron every 8 hours and 500 mg metronidazole every 12 hours) until discharge from the hospital. Pain control was achieved with hydromorphone hydrochloride delivered through a patient-controlled anesthesia device. Patients were discharged from the hospital when oral intake was adequate and pain well controlled without IV narcotics. Follow-up cross-sectional imaging (contrast-enhanced CT or PET/CT) was performed approximately 4-6 weeks after treatment of all tumor-bearing branches to evaluate response and determine the need for additional hepatic arterial chemoembolization treatments. If residual hepatic disease was present or if there was evidence of intrahepatic disease progression, additional chemoembolization procedures were performed with repeated imaging after repeated treatment of tumor-bearing vessels. Disease progression, response, and stability were defined according to the Response Evaluation Criteria in Solid Tumors [9]. Complications were evaluated with the National Cancer Institute Common Toxicity Criteria for Adverse Events (CTC) version 3.0, which is the accepted measurement tool for toxicity in oncologic studies [10]. Survival rates and time to disease progression from the time of first chemoembolization were calculated with Kaplan-Meier analysis.


Results
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 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 References
 
Patient Characteristics and Survival
Between February 2004 and February 2007, 20 patients (14 men, six women; mean age, 62 years; range 31-81 years) underwent 46 hepatic arterial chemoembolization procedures. Seventeen patients had ocular and three had cutaneous melanoma. All patients except one presented with bilobar disease with more than 10 tumors measurable on imaging. Most of the patients had too many tumors to count. The patient who was the exception had a solitary 8-cm tumor in the right lobe of the liver and was judged not a candidate for resection. One to five hepatic arterial chemoembolization treatments were performed per patient (mean, 2.4 treatments per patient). There were no deaths within 30 days of treatment and no complications according to CTC version 3.0 criteria. Kaplan-Meier analysis showed the mean and median overall survival times for the group were 334 ± 71 and 271 days, respectively (range, 36-1,185 days) (Fig. 1). Six patients were alive at the time of this writing, a median survival time of 311 days (range, 141-1,185 days).


Figure 3
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  		Fig. 3A —51-year old woman with metastatic ocular melanoma. Angiogram shows nodular metastatic ocular melanoma before therapy.

 


Figure 4
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  		Fig. 3B —51-year old woman with metastatic ocular melanoma. Pretreatment PET/CT scan shows hypermetabolic focus in right lobe of liver.

 


Figure 5
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  		Fig. 3C —51-year old woman with metastatic ocular melanoma. PET/CT scan after hepatic arterial chemoembolization shows metabolic activity in dominant tumor has been eliminated and replaced with dense uptake of iodized oil. Patient survived 427 days from first embolization session.

 
According to the Response Evaluation Criteria in Solid Tumors, there were no complete or partial responses. At initial follow-up, 13 (65%) of the patients had stable disease and seven (35%) had progression. All seven patients with progression at initial follow-up died within 109 days. Of the 13 patients with stable disease on initial imaging, six eventually had disease progression, for a total of 13 patients with progression of disease. The mean and median progression-free survival times for this group of patients were 231 ± 42 and 185 days, respectively (Fig. 2).

Angiographic Appearance
Review of angiographic images showed two distinct appearances of hepatic metastatic lesions. In one subset of patients (n = 8), large nodular well-defined tumor masses were present (Fig. 3A, 3B, 3C). In the other subset of patients (n = 12), a diffuse infiltrative staining pattern without distinct nodularity was seen (Fig. 4A, 4B). The cross-sectional imaging appearance was not predictive of the angiographic appearance.


Figure 6
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  		Fig. 4A —43-year-old man with metastatic ocular melanoma. Angiogram shows miliary pattern of contrast enhancement throughout liver without dominant nodules.

 

Figure 7
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  		Fig. 4B —43-year-old man with metastatic ocular melanoma. PET images 2 weeks before hepatic arterial chemoembolization suggest nodular appearance. This lack of correlation was common in patients with infiltrative angiographic appearance. Patient survived 45 days from first embolization session.

 
Kaplan-Meier analysis of the two distinct angiographic subsets revealed that angiographic appearance strongly correlated with and was predictive of survival and disease progression after hepatic arterial chemoembolization. Overall survival among patients with the nodular angiographic appearance was significantly longer than among the group with infiltrative findings (621 ± 87 vs 115 ± 22 days; p = 0.0002) (Fig. 5). The median survival times for the nodular and infiltrative groups were 750 and 109 days, respectively. All of the 35% of patients who had immediate disease progression despite hepatic arterial chemoembolization had the infiltrative angiographic pattern. The longest survival period of any patient with the infiltrative angiographic pattern was 271 days. Time to progression also was longer for patients with the nodular angiographic pattern, although this value did not reach statistical significance, likely because of sample size (nodular, 250 ± 62 days; infiltrative, 63 ± 8 days; p = 0.90) (Fig. 6).


Figure 8
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  		Fig. 5 —Graph shows overall survival period after hepatic arterial chemoembolization is significantly longer in patients with nodular pattern (dashed line) compared with patients with infiltrative pattern (solid line) of disease. Mean and median survival periods for nodular group were 621 ± 87 and 750 days and for infiltrative group were 115 ± 22 and 109 days (p = 0.0002).

 

Figure 9
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  		Fig. 6 —Graph shows results of Kaplan-Meier analysis of time to disease progression. Mean time to progression was 250 days for patients with nodular angiographic pattern (dashed line) and 63 days for patients with infiltrative pattern (solid line) (p = 0.5).

 

Discussion
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 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
References
 
Ocular melanoma represents less than 5% of all reported cases of melanoma but is the most common primary intraocular malignant tumor in adults and the second most common site of primary melanoma after cutaneous sources. Ocular and cutaneous melanomas both arise from the same embryologically derived dendritic melanocytes. The incidence of ocular melanoma is approximately six cases per 1,000,000 persons in the United States, with approximately 1,200-1,500 cases diagnosed each year. The average age at diagnosis is 55 years [3, 4]. More than one half of patients who undergo apparently successful therapy for the primary tumor eventually have distant hematogenous metastasis. Cutaneous melanoma is far more common than ocular melanoma, approximately 57,000 cases being diagnosed each year. Unlike ocular melanoma, however, cutaneous melanoma metastasizes through the lymphatic vessels to regional lymph nodes or by hematogenous spread to almost any organ [11-13]. The liver is the third most common organ involved. When they develop, hepatic metastatic lesions are rarely isolated and amenable to hepatic arterial chemoembolization. Other investigators (Ahrar et al., presented at the 2007 annual meeting the Society of Interventional Radiology) have presented data showing that the outcomes of hepatic arterial chemoembolization are comparable for ocular and cutaneous melanoma.

Ocular melanoma has a high affinity for metastasizing to the liver, which is usually the first site of extraocular disease and is involved in approximately 90% of patients. In more than one half of patients with metastatic disease, the liver may be the only organ involved [14, 15]. The presence of hematogenous metastasis in the liver is a major determinant of clinical course and patient survival. Despite advances in the diagnosis and management of primary uveal melanoma, hepatic metastasis remains refractory to standard oncologic therapies. Once hepatic metastasis is diagnosed, the mean survival time without treatment is only 2-3 months. Treatment with systemic chemotherapy is of limited value, the reported mean survival time being approximately 4 months [16-18]. Surgical resection is rarely an option. Although one study [19] showed an overall survival period of 27 months, less than 10% of patients with hepatic metastasis in that study were candidates for surgical resection.

In 1988, Mavligit et al. [2] first reported management of ocular melanoma with hepatic arterial chemoembolization and cisplatin and PVA particles. Those authors reported a 46% radiologic response rate and an 11-month median survival time for 30 patients with metastatic ocular melanoma. In 1995, the same group [6] reported their institutional experience comparing hepatic arterial chemoembolization, systemic chemotherapy, and hepatic arterial chemotherapeutic infusion through a surgically implanted port in the treatment of patients with meta-static ocular melanoma. Only hepatic arterial chemoembolization with the cisplatin-based regimen produced a meaningful response rate. Responders survived a median of 14.5 months; patients who underwent systemic therapy survived 5 months. Not all patients responded to chemoembolization; that subset survived a median of 5 months. This outcome is similar to that among our group of patients who did not respond to therapy.

Improved survival among patients with metastatic uveal melanoma managed with hepatic arterial chemoembolization and carmustine has been reported [7]. The overall median survival time in that study was 5.2 months. However, patients with a radiographic response had a median survival time of nearly 22 months. Another treatment option attempted is direct hepatic arterial chemotherapeutic infusion through a surgically implanted port. Using fotemustine, Leyvraz et al. [20] reported a response rate of 40% and a median overall survival time of 14 months. Feldman et al. [21] and Grover and Alexander [22] evaluated isolated hepatic perfusion by infusing melphalan and capturing the effluent from the hepatic vein. This treatment led to a radiologic response in approximately 60% of patients and resulted in a median survival period of 12 months. There is much room for improvement in maximizing the percentage of patients who respond and delaying the time to disease progression and treatment failure. Other catheter-directed techniques, such as use of 90Y have not been described but may be of value.

The results of the current study show overall mean and median survival times of 271 and 334 ± 71 days among patients with liver-dominant metastatic melanoma managed with cisplatin-doxorubicin-mitomycin hepatic arterial chemoembolization. We found that compared with the findings in studies of single-drug regimens, the multidrug regimen is extremely well tolerated without additional toxicity. The survival period of our group of patients is consistent with previously reported median survival times of 5 and 11 months with carmustine and cisplatin therapy, respectively.

An important finding of our study is recognition of two distinct angiographic patterns of metastatic melanoma that appear to be predictive of patient response and overall survival after hepatic arterial chemoembolization treatment. Patients with the nodular angiographic pattern were found to have a favorable response to hepatic arterial chemoembolization treatment, evidenced by a median survival time of more than 2 years. Patients with the infiltrative angiographic pattern, however, typically did not have a favorable response to hepatic arterial chemoembolization treatment, evidenced by a median survival time of only 115 days. We believe that the strong correlation between the observed angiographic pattern and survival benefit after hepatic arterial chemoembolization may be valuable prognostic information that can be used to help counsel and guide the care of individual patients. Unfortunately, the observed angiographic pattern was not accurately predicted with pretreatment contrast-enhanced CT or PET/CT.

Although it is possible that the nodular pattern may represent an earlier pattern of disease that eventually transforms into infiltrative disease, this evolution was not observed in our cohort. The nodular and infiltrative angiographic patterns may be related to underlying differences in tumor genetics that confer different biologic behavioral and growth patterns that result in the observed morphologic features. This hypothesis is supported by results of gene expression profile experiments showing that primary uveal melanomas cluster into two distinct molecular classes. Results of this molecular classification into distinct low-grade (class 1) and high-grade (class 2) groups are strongly predictive of metastatic death of patients with ocular melanoma [4, 23-25]. It is tempting to speculate that the differences in molecular class may be related to the differences in angiographic pattern and response to hepatic arterial chemoembolization treatment. To further investigate this possibility, we are obtaining hepatic arterial chemoembolization before hepatic biopsy specimens for gene profile analysis.

Deficiencies of this study were those inherent to a retrospective design and those related to small sample size. Our sample size, however, was similar to those in other studies of hepatic arterial chemoembolization [2, 7]. Given the size of the study group, we use these findings as a way to counsel patients, not to make decisions about whether therapy should be offered. Our treatment group did include two types of melanoma, but Ahrar et al. (presented at the 2007 annual meeting the Society of Interventional Radiology) found similar survival data among patients with differing melanotic sources. The number of patients with cutaneous melanoma in our group was too small for statistical comparison with those with ocular melanoma. However, the patients with cutaneous melanoma were not outliers in median survival. The only two patients who survived more than 1,000 days in our group had ocular melanoma.

Ocular melanoma is a rare tumor, and once hepatic metastasis is diagnosed, patients are faced with an extremely poor prognosis. Hepatic arterial chemoembolization of hepatic metastatic lesions of melanoma was first reported in the late 1980s and has been found to be a safe, well-tolerated treatment option. Unlike the well-reported outcome of hepatic arterial chemoembolization for hepatocellular carcinoma, there is a relative lack of information in the medical literature on outcome after hepatic arterial chemoembolization therapy for metastasis of hepatic melanoma. In this study, we found improved survival among patients with metastatic melanoma managed with cisplatin-doxorubicin-mitomycin C hepatic arterial chemoembolization compared with survival of historical controls treated with systemic chemotherapy and suggest that this outcome can be predicted on the basis of angiographic pattern.


References
Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 

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P. N. Dayani, J. E. Gould, D. B. Brown, K. V. Sharma, G. P. Linette, and J. W. Harbour
Hepatic Metastasis From Uveal Melanoma: Angiographic Pattern Predictive of Survival After Hepatic Arterial Chemoembolization
Arch Ophthalmol, May 1, 2009; 127(5): 628 - 632.
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