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Annals of Surgical Oncology 9:762-770 (2002)
© 2002 Society of Surgical Oncology

ORIGINAL ARTICLES

The Surgical Management of Metastatic Melanoma

Peter J. Allen, MD and Daniel G. Coit, MD

From the Department of Surgery, Memorial Sloan-Kettering Cancer Center, New York, New York.

Correspondence: Address correspondence and reprint requests to: Daniel G. Coit, MD, Gastric & Mixed Tumor Service, Department of Surgery, Memorial Sloan-Kettering Cancer Center, 1275 York Ave., New York, NY 10021; Fax: 212-717-3400; E-mail: coitd{at}mskcc.org


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 SURGICAL MANAGEMENT OF...
 CONCLUSIONS
 REFERENCES
 
Abstract: When deciding whether or not to perform a resection for metastatic melanoma, one should follow general principles that apply to the patient with melanoma as well as to the patient with metastases from other types of primary tumors. When the resection is palliative, the success of surgical treatment will be governed by the presence of identifiable symptoms, the morbidity of the procedure, the course of the disease, and the ability to communicate treatment goals among surgeon, patient, and family. When the resection is performed with curative intent, long-term survival depends on the ability of the surgeon to select patients with a pattern of recurrence suggestive of a less aggressive tumor biology. Regardless of the extent of the operative procedure, resection of metastases in patients whose disease recurs early after the treatment of the primary tumor, in those who present with multiple lesions, and in those who present with disease that cannot be completely resected will only rarely be associated with subsequent long-term survival.

Key Words: Melanoma • Metastasis • Soft tissue • Lymph nodes • Lung • Gastrointestinal tract


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
SURGICAL MANAGEMENT OF...
 CONCLUSIONS
 REFERENCES
 
After treatment of the primary lesion, melanoma will recur in approximately one third of patients. Melanoma can recur in almost every major organ and tissue in the body.1 The risk of recurrence is directly related to the stage at presentation. When nodal or distant metastases are absent, stage is determined by the thickness of the primary lesion and whether or not the primary lesion is ulcerated.2 Regional nodal metastases are the most common site of recurrence. Patients with primary lesions from .76 to 1.5 mm thick have up to a 25% chance of developing a regional nodal recurrence within 3 years.3 Patients with primary lesions from 1.5 to 4 mm thick have up to a 60% chance of developing nodal metastases within 3 years. Distant sites of metastasis are less common, but their occurrence is also directly related to the thickness of the primary lesion. Patients with primary lesions from 1.5 to 4 mm thick have a 15% chance of developing distant metastases within 5 years of diagnosis.

The site of initial recurrence is an important predictor of survival. Most patients who experience recurrence with regional nodal disease will undergo lymphadenectomy, and 5-year survival rates between 20% and 50% have been reported.4–6 Patients whose disease recurs at distant sites, both visceral and nonvisceral, have 5-year survival rates of approximately 5%.7–9 Most patients with distant recurrence are not candidates for curative resection and are often treated with chemotherapy, immunotherapy, or radiotherapy.

Patients with distant metastases who are selected for curative resection likely represent those with improved performance status and less aggressive tumor biology. The selection of patients with a pattern of recurrence that may benefit from resection is critical. No matter how extensive the resection, patients with early recurrence at multiple sites will do poorly. Complete resection, however, has been the only form of treatment for metastatic disease that has been consistently associated with any actual 5-year survival and should be considered when appropriate.9–11

Because the initial site of distant recurrence has been found to be predictive of survival, the American Joint Committee on Cancer has proposed changes in the classification of metastatic disease (M classification) on the basis of the site of recurrence.2,10,12,13 Patients with nonvisceral metastases (soft tissue, distant nodal) have been reported to have a better prognosis than patients with visceral metastases, and in the proposed classification system they have been classified as having M1 disease (Table 1). Some series have also suggested that patients with pulmonary metastases, either resected or nonresected, may experience better survival than patients with visceral metastases at other sites, and these patients have been classified as having M2 disease.7,10 Regardless of the site of distant metastasis, the presence of increased lactate dehydrogenase (LDH) has been found to be among the most important predictors of poor outcome, and therefore patients with increased LDH have been classified as having M3 disease, along with patients who develop nonpulmonary visceral metastases.14,15


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  		TABLE 1. TNM classification for melanoma as proposed by the AJCCa
 

   SURGICAL MANAGEMENT OF METASTATIC DISEASE
TOP
 ABSTRACT
 INTRODUCTION
 SURGICAL MANAGEMENT OF...
CONCLUSIONS
 REFERENCES
 
When evaluating a patient for resection of metastatic melanoma, one must first define whether the goal of the operation is palliative or curative. Palliative resection for malignancy has been infrequently studied; however, a recent review found that 12.5% of all surgical procedures performed at a dedicated cancer center were for palliative reasons.16 Palliative procedures must be accomplished with minimal morbidity, essentially no mortality, and a limited hospital stay, and must address a specific symptom. Also critical to the success of palliative surgery is that the goals of the given operation be clearly understood by patient, family, and surgeon. Relief of symptoms after palliative resection for metastatic melanoma has been reported to occur in 77% to 100% of patients, depending on the site and reason for resection.17

When considering a patient for curative resection, there are a number of tumor-related factors that should be considered. These factors, which have been found to be predictive of survival after metastatic resection, should be considered as surrogates for tumor biology. Cady18 has put forth basic principles in surgical oncology that apply to the patient with metastatic melanoma as well as to the surgical treatment of malignant disease in general. These principles are the following: "In the field of surgical oncology tumor biology is king, patient selection is queen, and technical maneuvers are the prince and princess who try, but usually fail, to usurp the throne."

When considering patients for resection of metastatic melanoma, one must carefully select those whose pattern of recurrence suggests a tumor biology that is likely to benefit from resection. Regardless of the extent of resection, patients with metastatic melanoma and multiple negative predictors of survival are unlikely to achieve long-term survival.

Factors that have often been cited as predictive of survival after complete metastatic resection include the site of metastasis, the number of metastatic lesions, and the disease-free interval (DFI) before the development of metastases. These three tumor-related factors are representative of tumor biology and are predictors of outcome independent of the magnitude of the resection. The DFI before the development of metastasis has been found to be predictive of survival in multiple studies evaluating all sites of recurrence.7,8,11,19 Recurrence within 1 year of treatment of the primary tumor has been found to be highly predictive of poor outcome. Most studies evaluating the predictive nature of the number of metastatic deposits have investigated pulmonary recurrence, with significantly worse survival after resection of more than one or two metastases.11,19,20 The site of metastasis, whether visceral or nonvisceral, and, if visceral, pulmonary or nonpulmonary, has been found to be predictive of outcome in numerous studies, and on the basis of these observations, the American Joint Committee on Cancer has proposed a change in the classification of metastatic disease (M).2

The importance of careful patient selection should not be underestimated. Its importance is exemplified in a recent article evaluating the resection of metastatic melanoma to the liver in patients presenting to the John Wayne Cancer Institute and the Sydney Melanoma Unit.21 In general, patients with melanoma who develop hepatic metastases are considered to have unresectable disease, because most will have either disseminated hepatic disease or disease at other distant locations at the time of diagnosis. In the study from the John Wayne Cancer Institute, however, a 5-year survival of 29% was reported for patients undergoing complete resection of hepatic metastases. In the time period of this study, 26,204 patients with melanoma were seen, of whom 1,750 patients (7%) had hepatic metastases. Resection was attempted in only 34 of the 1750 patients (2%) who presented with, or developed, hepatic metastases. The median DFI to the development of hepatic metastases in this group of patients was 58 months, and 75% of patients had a solitary metastasis. Extensive intra-abdominal or hepatic disease prevented complete resection in 16 (47%) of the 34 patients who underwent exploration. Although the overall survival in this highly selected group of patients was reported to be 29%, at the time of last follow-up, only 5 (27%) of 18 patients who had undergone complete resection were without evidence of disease. In this study, through careful selection, 2% of patients with hepatic metastases underwent exploration, and at the time of last follow-up, five of the patients (.3% of patients with liver metastases) had experienced long-term disease-free survival.

The only treatment-related factor that has been consistently found to predict survival is complete resection. Without a complete resection, the procedure rarely alters the natural history of disease. In a study by Leo et al.,11 complete resection of pulmonary metastases was predictive of survival, with 22% and 16% of patients undergoing complete resection surviving 5 and 10 years, respectively. None of the 46 patients in this study who had an incomplete resection survived 5 years. Similar findings have been reported after resection of metastases to other sites as well. A study from our institution22 found complete resection to be predictive of survival after resection of gastrointestinal (GI) metastases, and an article by Ollila et al.23 evaluating surgical resection of recurrent stage IV melanoma at all sites also found complete resection to be associated with improved survival.

To select the most appropriate patients for resection, one must consider the predictors mentioned previously and perform a thorough preoperative staging evaluation. This evaluation is to ensure that no other sites of distant disease exist and that complete resection of the recurrence can be achieved. The work-up should include a thorough history, physical examination, and laboratory evaluation. Laboratory studies should include an LDH level. Radiographical evaluation should include a computed tomography (CT) scan of the chest, abdomen, and pelvis. Radiographical evaluation for bony metastasis is probably warranted only in symptomatic patients, because most patients with bony metastases will have pain, and performing a bone scan in all patients has been found to have a false-negative rate as high as 15% and a false-positive rate of approximately 20%.24,25 Likewise, radiographical evaluation for central nervous system (CNS) metastases is also warranted only in symptomatic patients, because the yield for detecting metastases in the asymptomatic patient is extremely low.26,27

Recently, interest has focused on the ability of positron emission tomography (PET) to more accurately detect occult metastatic deposits and therefore allow better selection of patients for metastatic resection. In one study by Jadvar et al.,28 38 patients with primary and recurrent melanoma were evaluated with CT and with PET. Compared with PET, the extent of disease was underestimated by the CT scan in five patients (13%). Additionally, in two cases, resection of metastatic disease was canceled because PET revealed additional sites of disease. The utility of PET in this setting has yet to be fully validated in prospective clinical trials. Although all of the predictors noted previously should be considered when deciding to perform metastatic resection, a clinically useful technique is to approach the patient by site of recurrence.

Remote Skin, Soft Tissue, and Lymph Nodes
The most common sites of initial distant recurrence for patients with melanoma are the skin, subcutaneous tissues, and distant lymph nodes.7,29 In a study by Balch et al.7 of 200 patients with metastatic melanoma, the skin and distant lymph nodes were the site of initial recurrence in 59% of patients. This underscores the need for careful physical examination when observing patients with a history of melanoma.

Resection of soft tissue and distant nodal recurrence can usually be performed with minimal morbidity and should be performed in both the curative and palliative settings. After curative complete resection of metastases in these sites, median survival has been reported to be 8 to 50 months, with 5-year survival rates of 5% to 38% (Table 2). The factor found to be most consistently predictive of survival in these patients has been the DFI, with patients who experience recurrence within 12 to 18 months of primary resection experiencing significantly worse survival than those disease recurs later. Palliative resections should also be considered, because the resection of symptomatic lesions can be performed relatively easily and with minimal morbidity.


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  		TABLE 2. Survival after complete resection of remote skin, soft tissue, and lymph node metastases in patients with melanoma
 
Pulmonary Metastases
Pulmonary metastases are the second most common site of metastasis, with 15% to 36% of clinically evident distant recurrence occurring in this location.7,33 The annual probability of developing pulmonary recurrence increases progressively from approximately 10% at 5 years to nearly 30% at 20 years.20 The long-term survival for patients with pulmonary metastases is poor, with only 4% of all patients with pulmonary metastases surviving 5 years.20 For patients who present with pulmonary metastases that are amenable to surgical resection, however, 5-year survival rates of >20% have been reported (Table 3).


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  		TABLE 3. Survival after complete resection of pulmonary metastases in patients with melanoma
 
Patients with pulmonary metastases most often present with an asymptomatic nodule discovered on follow-up chest x-ray.20,33,40 Patients with a history of melanoma who present with a new solitary pulmonary nodule on screening chest x-ray are more likely to have recurrent melanoma than either a primary lung malignancy or a benign process.41 Some studies evaluating solitary pulmonary nodules in patients with a history of melanoma, however, have found that as many as 30% to 50% of these patients will have either a benign diagnosis or a primary lung cancer.35,42 Although tissue is essential to establish the diagnosis, the size of the abnormality may be helpful in predicting whether the lesion will be benign or malignant. One study of 181 resection specimens from 41 patients with solitary pulmonary nodules and a history of extrapulmonary malignancy (including melanoma) found 90% of lesions >5 mm in size to be malignant, as compared with 33% of lesions <5 mm in size.43

Most patients with melanoma who have recurrence within the lung will not have surgically resectable lesions.9,10,20 A recent study by Leo et al.11 illustrates the importance of patient selection on the ability to achieve long-term survival. This study reviewed 328 patients who had undergone resection of metastatic melanoma to the lung. Most patients (65%) had a solitary metastasis, and the average DFI was 53 months. Complete resection was performed in 282 patients (86%). Within this highly selected group of patients (one to two metastases and a long DFI), the overall 5-year survival rate was 18%. At the time of last follow-up, 180 (64%) of the 282 patients who had undergone complete resection had recurrence; the most common site of re-recurrence was within the brain. None of the patients survived 5 years after complete resection.

The three factors most often reported as predictive of survival after pulmonary resection for metastatic melanoma are the ability to achieve complete resection, the number of metastases, and the DFI.11,20,39 Overett and Shiu,30 Harpole et al.,20 Tafra et al.,39 and Leo et al.11 have found that having more than one metastasis is an independent predictor of poorer survival; Marincola and Mark,37 Harpole et al.,20 and Leo et al.11 found that a prolonged DFI is associated with improved survival (Table 3). Although the DFI found to be predictive of improved survival differed in the studies, all found that the development of pulmonary metastases within a year of diagnosis was an independent negative predictor of survival. Leo et al. grouped the three independent predictors into the following three groups:

  1. Group 1: complete resection, DFI >36 months, single metastasis.
  2. Group 2: complete resection and either DFI <36 months or multiple metastases.
  3. Group 3: incomplete resection.

The survival difference among these groups was highly significant, with 5-year survival rates of 29%, 20%, and 7% in groups 1, 2, and 3, respectively.11

The fact that a small proportion of patients will never recur after complete resection of pulmonary metastases suggests that surgery most likely does influence the natural history of the disease in this highly selected minority of patients. Long-term durable complete responses are rarely achieved by any other form of treatment, and margin-negative excision has been found in multiple studies to be a very powerful predictor of survival.11,36 These studies have shown that even when DFI is long and only a solitary metastasis is present, if the lesion is not completely removed, 5-year survival is almost never achieved. In addition, Harpole et al.20 found significantly improved survival in patients with solitary metastasis who underwent curative resection (20% 5-year survival) as compared with patients with solitary metastasis who did not undergo resection (4% 5-year survival).

In summary, most patients who develop pulmonary metastases will not be candidates for surgical resection, and these patients have a 5-year survival of <5%. Because these patients are rarely symptomatic, pulmonary resection is usually performed with curative intent. Patients should be selected for surgery who present with a pattern of recurrence that predicts a survival benefit from resection. Long-term survival may be achieved in up to 20% of patients when resection is performed on patients who present with solitary lesions that develop >1 year after initial treatment.

Visceral (Nonpulmonary) Metastases
GI Tract
Only 2% to 4% of patients with melanoma will be diagnosed with GI metastasis during the course of their disease.44,45 Although the GI tract is an uncommon site of metastasis, melanoma is one of the most common tumors to metastasize to the GI tract and represents approximately one third of all GI metastases.46 The most common sites of GI metastases from melanoma include the small bowel (35%–67%), colon (9%–15%), and stomach (5%–7%).44,47

Most patients with GI metastases are symptomatic. Most patients will present with complaints suggestive of obstruction or bleeding.32,47,48 Patients with a history of melanoma and chronic anemia should be evaluated for the presence of GI metastasis. The evaluation of these patients should include upper and lower GI contrast studies, endoscopy, and CT. Because the sensitivity of these studies has been reported to be only 55% to 65%, a PET scan has been advocated by some as a potential method for identifying additional occult disease.48

Because most patients with GI metastasis will be symptomatic, surgical resection for palliative intent is often indicated even in the presence of extra-GI disease. In a recent study by Ollila et al.47 of 124 patients with GI metastases, 69 (55%) underwent operative exploration. Palliative resections were performed on 23 patients (34%). Presenting symptoms were relieved in 67 (97%) of the 69 patients who underwent resection, and there was only a single death and a single major postoperative complication. The high probability of symptomatic relief in patients with GI metastases, with minimal morbidity and mortality, has been duplicated at our institution and others. In a study from Memorial Sloan-Kettering Cancer Center of 68 patients with metastatic melanoma to the GI tract, 90% of patients were relieved of symptoms with a postoperative morbidity and mortality rate of 8.8% and 2.9%, respectively.22 In addition, an Australian study by Khadra et al.49 of 56 patients with metastatic melanoma to the GI tract reported relief of symptoms in 79% of patients who had undergone palliative resection.

Long-term survival in subsets of patients with metastatic melanoma to the GI tract has been documented. The factor found to be most predictive of survival is the ability to perform a complete resection. Ricaniadis et al.48 reported a study of 47 patients who underwent resection of metastatic melanoma to the GI tract. The median survival was 28 months for patients who had undergone complete resection, compared with 5 months for patients who had undergone incomplete resection. Other factors reported to be predictive of survival include the DFI and the preoperative LDH level.

In summary, most patients diagnosed with metastatic melanoma to the GI tract will be symptomatic. Palliative resection for GI metastases can be performed with minimal morbidity and mortality and will relieve symptoms in up to 90% of patients. When no extra-GI disease exists and complete resection can be accomplished, long-term survival may be achieved in a minority of patients.

Brain
Approximately 8% to 15% of melanoma patients will be diagnosed with CNS metastases during the course of their disease.50 Autopsy evidence, however, reveals that 50% to 80% of patients who die from melanoma have CNS metastases at the time of death.51,52 Although any site may be involved, the most common sites of CNS metastasis are the cerebral hemispheres (75%–86%) and the cerebellum (10%–15%).53–55

As autopsy studies would indicate, few patients with CNS metastases from melanoma will develop symptoms, and therefore, in the absence of routine radiographical evaluation, only a few patients will be diagnosed before death. Symptoms of CNS metastasis are those that are suggestive of a space-occupying lesion, such as headache, neurological deficit, or seizure. The work-up for these patients includes standard imaging by CT and magnetic resonance imaging.

The local treatment options for patients with CNS metastasis include whole-brain radiation, stereotactic radiosurgery, and surgical resection. Because of the lack of efficacy and the cognitive and behavioral complications of whole-brain radiation, recent clinical studies have focused on stereotactic radiosurgery.54–57 In one study by Lavine et al.,55 45 patients with metastatic melanoma to the brain underwent stereotactic radiosurgery. The location of these lesions was cortical in 86% of patients; 51% of treatments were to a single lesion, and the mean treatment volume was 5.6 cm3. Extracranial visceral metastases were present in 77% of the patients. After treatment, 78% of patients experienced either improved or stable neurological symptomatology, and only 16% of patients experienced significant complications (seizures in four patients and transient worsening of preprocedural paresis in three patients). Follow-up imaging studies revealed a 97% rate of local tumor control, and 28% of lesions disappeared radiographically. Despite these encouraging results, the palliative nature of this procedure is exemplified by the overall median survival of 8 months. Similar results have been found in other studies, and presently stereotactic radiosurgery is considered an effective noninvasive means of providing palliation with minimal morbidity in patients with one or two small metastases that are not amenable to surgical resection.

Surgical resection is performed in the minority of patients, and even in these cases the procedure is most often palliative in intent.58,59 In the largest study reported on surgical resection of brain metastases, by Wronski and Arbit,53 the importance of careful patient selection was again emphasized. In this study of 91 patients who underwent surgical resection of metastatic CNS melanoma, 76 patients (84%) had a single lesion, and the median DFI was 14 months. In this study, 49 patients underwent whole-brain radiation after resection, and the addition of this modality did not change the rate of local recurrence or survival. The median survival of all patients after resection of brain metastasis was 7 months, with a 5-year survival of 7%.

In summary, patients who develop metastatic melanoma to the brain have a very poor prognosis, with a median survival of approximately 6 months regardless of treatment. Most patients treated for symptomatic lesions will have either incomplete removal of CNS disease or will have spread in other distant locations, and therefore, in the majority of cases, resection should be considered palliative. Most patients selected for treatment with either stereotactic radiosurgery or craniotomy, however, will experience either an improvement or stabilization of their symptoms, with minimal morbidity.

Adrenal
Recently, long-term survival after adrenalectomy for metastatic melanoma has been reported.60,61 In the largest series out of the John Wayne Cancer Institute, a database of 8250 patients with melanoma was reviewed.61 Within this database, 83 cases of adrenal metastasis were discovered. Most of these patients (56 patients) were treated nonoperatively. Surgical exploration was performed on 27 patients (33%), with 18 of these patients undergoing a complete resection. The median survival of patients who had undergone complete resection was 26 months, and for patients who had undergone an incomplete resection, the median survival was 9 months.

In the study from the John Wayne Cancer Institute, patients underwent CT scan of the chest, abdomen, and pelvis; magnetic resonance imaging of the brain; and, in some instances, PET scanning as evaluation for additional sites of metastasis before adrenal resection. The average DFI before the adrenal metastasis was 25 months, and 37% of patients undergoing exploration had the adrenal gland as their initial site of distant recurrence. Similar results have been reported from Duke University, as well as our own institution, and probably represent our increasing ability to select patients with tumor biology most amenable to metastatic resection.60,62

In summary, given the overall poor prognosis of patients with stage IV melanoma and the ineffectiveness of nonsurgical therapies, patients who present with isolated adrenal metastasis and who are without significant comorbidity may benefit from adrenal resection.

Other Sites
The two other most common sites of distant recurrence mentioned in the surgical literature are the heart and the liver. Multiple case reports exist of patients with a history of melanoma who present with cardiac symptoms (most often syncope) and who are found on echocardiography to have intracardiac lesions.63,64 When technically feasible, these resections should be considered as palliative, because long-term survival is yet to be reported. As noted previously, almost all patients who present with metastatic melanoma to the liver will present with disseminated disease; however, case reports and now a single series have been reported of patients with solitary lesions, usually from ocular melanoma, who have undergone resection.65,66 One of these case reports described a patient with uveal melanoma who developed a solitary hepatic metastasis 25 years after treatment of the primary tumor.65 Regardless, long-term survival after resection of metastatic melanoma to the heart or liver remains largely anecdotal.


   CONCLUSIONS
TOP
 ABSTRACT
 INTRODUCTION
 SURGICAL MANAGEMENT OF...
 CONCLUSIONS
REFERENCES
 
In conclusion, surgical resection is an important component to be considered in the treatment of patients with metastatic melanoma. When specific symptoms exist and complete resection cannot be achieved, operative treatment must be considered palliative. In this setting, the goals of the operation should be carefully explained to the patient and family. Local palliative excision for distant skin and nodal recurrence is associated with minimal morbidity and should be performed. Metastases to the GI tract may also be resected, with morbidity rates as low as 8% and associated relief of symptoms in >90% of patients.18,22,47 Acceptable results for the palliative resection of brain metastasis have also been reported; however, in the setting of disease not accessible to surgical resection, stereotactic radiosurgery may provide equivalent rates of symptom relief with less morbidity.53–57

When curative resection of metastatic disease is contemplated, the patient should undergo the appropriate physical and radiographical examination to evaluate for other sites of distant disease and to confirm that complete resection can be performed. When these criteria can be met, the selection of patients with a longer DFI before the development of metastasis and fewer numbers of metastatic deposits may result in 5-year survival rates of up to 25%. Technical feats in poorly selected patients with negative predictors of long-term survival will rarely result in a significant alteration in the natural history of biologically aggressive disease (Table 4).


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  		TABLE 4. Survival after complete resection of visceral metastases in patients with melanoma
 


   Footnotes
 
Complete surgical resection of metastatic melanoma with curative intent may alter the natural history of patients with less aggressive tumor biology, such as those with a solitary site and a prolonged clinical course. Surgical resection of metastatic melanoma with palliative intent is often effective in relieving identifiable symptoms in carefully selected patients.

Received for publication February 15, 2002. Accepted for publication May 21, 2002.


   REFERENCES
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 ABSTRACT
 INTRODUCTION
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