INTRODUCTION — Although the incidence of malignant melanoma is increasing, most cases are diagnosed at an early stage. In that setting, surgical excision is curative in most cases, and patients at high-risk of developing metastatic disease may benefit from adjuvant therapy with interferon alpha [1]. (See "Initial surgical management of melanoma of the skin and unusual sites" and "Adjuvant interferon alfa for intermediate- and high-risk melanoma".)
Most patients with stage IV disease (table 1A-B) require systemic treatment. Immunotherapy with ipilimumab, an anti-CTLA4 (cytotoxic T lymphocyte-associated antigen 4) antibody, significantly increases overall survival in patients with advanced melanoma who have failed on previous systemic therapy and has been approved for use in patients with metastatic or unresectable melanoma. The efficacy and toxicity profile of ipilimumab in patients with advanced melanoma will be reviewed here.
CHOICE OF THERAPY FOR DISSEMINATED DISEASE — Approaches that have been shown to provide clinically important benefit for patients with disseminated melanoma in appropriately selected patients include immunotherapy with high-dose interleukin-2 (IL-2), immunotherapy with ipilimumab, a monoclonal antibody targeting CTLA-4, and inhibition of the MAP kinase pathway with vemurafenib in patients whose tumors contain a V600 mutation in the BRAF gene.
There are no randomized trials that compare these different approaches and there are no data on the appropriate sequencing of these therapies. Until such data are available, the choice of treatment needs to be individualized. Treatment decisions depend upon multiple factors including the overall condition of the patient (eg, age and comorbidity), a molecular analysis for the presence of a V600 mutation in the BRAF gene, and the extent of metastatic disease.
RATIONALE — Activation of cellular immunity begins when T cells recognize peptide fragments of intracellular proteins that are expressed on the surface of antigen presenting cells bound to specific MHC molecules. This interaction requires the presence of a costimulatory molecule (B7).
The CTLA-4 receptor on T lymphocytes is a negative regulator of T cell activation that outcompetes CD28 for binding to B7 on antigen presenting cells. CTLA-4 thereby serves as a physiologic “brake” on the activated immune system. Ipilimumab is a monoclonal antibody to CTLA-4 that can prevent this feedback inhibition, resulting in an unabated immune response against the tumor. In addition, this interaction can cause a breaking of tolerance to other host tissues that leads to potentially severe or even life threatening autoimmune adverse events.
EFFICACY OF IPILIMUMAB — Evaluation of the effectiveness of ipilimumab therapy, both in clinical trials and in individual patients, requires an understanding of the different patterns of response seen with this class of agents.
Patterns of response — The observed patterns of response to treatment with ipilimumab differ from those with cytotoxic chemotherapy or molecularly targeted agents in several important respects [2]:
Immune-related response criteria have been proposed to deal with the altered patterns of response seen with ipilimumab and potentially other immunotherapies [2].
The use of these immune-related response criteria are important because the application of traditional RECIST criteria (table 2) in patients treated with ipilimumab may lead to premature discontinuation of treatment in a patient who will eventually respond to treatment.
Impact on survival — Based upon results from phase I and phase II studies, two major phase III trials have been conducted.
Previously treated patients — Ipilimumab was studied in a placebo-controlled phase III trial, in which 676 patients were randomly assigned in a 3:1:1 ratio to ipilimumab plus a glycoprotein 100 (gp100) vaccine, ipilimumab alone, or gp100 alone [3]. All patients were HLA-A*0201 positive and had unresectable metastatic melanoma. All patients had received prior systemic treatment for advanced disease with either cytotoxic chemotherapy or interleukin-2.
Ipilimumab (3 mg/kg) and/or vaccine were given every three weeks for four doses. Patients with confirmed partial or complete response or stable disease for three months or more after completion of the 12 week induction period were allowed to receive reinduction with their original treatment if they subsequently had disease progression. The primary endpoint of the trial was overall survival.
Key results of this trial included the following:
The phase III trial limited enrollment to patients who were HLA-A*0201 positive because of the use of the gp100 vaccine [3]. Retrospective analysis of 453 previously treated patients treated with ipilimumab in four phase II trials compared patients who were HLA-A*0201 positive with those who were HLA-A*0201 negative [4]. In this analysis, ipilimumab had similar activity regardless of HLA type.
Patients with untreated brain metastases were excluded from the phase III trial [3]. Other studies and case reports have observed antitumor activity with ipilimumab treatment in patients with brain metastases. (See "Systemic therapy for brain metastases", section on 'Melanoma'.)
Previously untreated patients — In a second phase III trial, 502 patients with metastatic melanoma were randomly assigned to ipilimumab plus dacarbazine or to placebo plus dacarbazine [5]. Approximately one-fourth of patients had received prior adjuvant therapy, but those previously treated for metastatic disease were not eligible. Patients with brain metastases, ocular melanoma, mucosal melanoma, or autoimmune disease were excluded.
All patients received dacarbazine (850 mg/m2 intravenously) every three weeks for eight cycles in the absence of disease progression or significant toxicity. Patients were randomly assigned to receive either ipilimumab at a dose of 10 mg/kg or placebo on weeks 1, 4, 7, and 10. At week 24, patients with stable disease or an objective response were eligible for maintenance therapy with ipilimumab at 10 mg/kg or placebo given every twelve weeks.
Major results of this trial include the following:
Whether this blunting of immune toxicity by dacarbazine might have also blunted the antitumor effect of ipilimumab is a matter of speculation. However, the overall pattern of toxicity and efficacy on this trial do not support the addition of dacarbazine to ipilimumab nor the use of ipilimumab at the 10 mg/kg dose compared with the approved 3 mg/kg dose.
Long-term duration of response — Although only a minority of patients achieve a complete response, such responses appear to be durable and of prolonged duration in most cases. As an example, in the composite experience from the National Institutes of Health, 177 patients were treated with ipilimumab in three studies between 2002 and 2005 [6]. Nearly 9 percent of treated patients experienced a complete response of which all but one have lasted between 54 and 99 months. The responses could be very delayed in developing, in some cases even after 30 months. The complete responses were most frequent in those who received interleukin-2 with the ipilimumab.
Brain metastases — Preliminary results from phase II studies indicate that ipilimumab has activity in patients with brain metastases and that its safety profile in those patients is similar to that in patients without brain metastases. (See "Management of brain metastases in melanoma", section on 'Immunotherapy'.)
Dose and schedule — Ipilimumab has been studied at different doses and schedules. The approved dose of ipilimumab is 3 mg/kg by intravenous infusion given every three weeks for four doses based upon the results of the phase III trial in previously treated patients [3]. More recent protocols for which results are not yet available have used ipilimumab at a dose of 10 mg/kg by intravenous infusion given every three weeks for four doses with maintenance ipilimumab at 10 mg/kg provided every 12 weeks. (See 'Impact on survival' above.)
Three dose levels of ipilimumab were compared in a double-blind phase II trial, in which 217 patients with advanced melanoma were randomly assigned to one of three dose levels: 0.3 mg/kg, 3.0 mg/kg, and 10 mg/kg [7]. Patients were treated every three weeks for four cycles, with provision for maintenance treatment every 12 weeks in patients with an objective response or stable disease.
There was an increase in the frequency of adverse events at increasing dose levels, particularly for those events considered immune-related:
In some protocols, patients with an objective tumor response or stable disease after the induction period could receive an additional dose every 12 weeks as “maintenance therapy” as tolerated until disease progression. In other trials, including the initial phase III [3], patients did not receive routine maintenance therapy; however, those exhibiting disease progression after having disease response or stable disease following the induction period were allowed to undergo “reinduction” according to the same schedule if they subsequently progressed.
Future directions — The EORTC melanoma group is conducting a phase III trial in patients with high-risk stage III disease (EORTC 18071, NCT00636168) [8]. In this trial, patients are being randomly assigned to ipilimumab (dose 10 mg/kg every three weeks for four cycles then every 12 weeks for a total of three years treatment) or to placebo following complete resection to determine whether such treatment can prevent disease recurrence [9].
In addition, a cooperative group trial comparing ipilimumab to interferon alpha in patients with resected stage IIIB, IIIC or IV disease is anticipated to start in the United States in mid 2011 (NCT01274338) [8].
Clinical trials will be required to ascertain the role of ipilimumab compared with molecularly targeted therapies in patients with tumors possessing characteristic mutations in BRAF. (See "Molecularly targeted therapy for metastatic melanoma".)
TOXICITY OF IPILIMUMAB — Ipilimumab’s presumed mechanism of action is to break down tolerance to tumor-associated antigens in the melanoma. At the same time, this break down of tolerance may result in autoimmune reactions against self antigens. A wide range of immune-mediated adverse events have been observed. The most common serious manifestations include enterocolitis, hepatitis, dermatitis, and endocrinopathies. (See 'Rationale' above.)
In the phase III trial that demonstrated an increase in survival, immune-related adverse events occurred in approximately 60 percent of patients treated with ipilimumab; these typically did not occur until several weeks into therapy [3]. Overall, severe or life-threatening (grade 3 or 4) toxicity was seen in 10 to 15 percent of ipilimumab-treated patients, compared to 3 percent in those receiving only gp100. The phase III trial used a dose of 3 mg/kg of ipilimumab every three weeks. A somewhat higher incidence of side effects was observed with a dose of 10 mg/kg every three weeks in the randomized phase II trial that assessed the effects of dose on activity and toxicity [7]. (See 'Dose and schedule' above.)
Treatment of immune-mediated toxicity — Phase II and phase III trials have shown that prompt medical attention and early administration of corticosteroids are essential for the management of immune-related adverse events and to prevent their progression to more serious toxicity [3,7,10,11]. The Food and Drug Administration (FDA) has created a Risk Elimination and Management System (REMS) to provide additional information to both healthcare providers and patients, which is available on the internet [12,13].
Treatment requires interruption of ipilimumab and the use of corticosteroids [14]. Treatment is based upon the severity of the observed toxicity:
Enterocolitis — Diarrhea and/or colitis are among the most common, and potentially most serious, complications of anti-CTLA4 treatment. In the phase III trial, diarrhea and/or colitis was reported in 31 percent of cases, of which 6 percent were serious or life-threatening [3]. Although the clinical presentation is similar to that with inflammatory bowel disease, the distribution of lesions and histopathology are not characteristic of Crohn’s disease or ulcerative colitis [15].
Symptoms of colitis can develop rapidly and become life-threatening [16-19]. Bowel perforation, sepsis, and death have been reported as complications of ipilimumab therapy [16,19,20]. In the phase III trial, the median time to development of moderate or severe enterocolitis after initiating ipilimumab therapy was six to seven weeks [14].
Meticulous attention to gastrointestinal symptoms is required to prevent progression to more serious complications [14]. Patients should be monitored for symptoms of enterocolitis (diarrhea, abdominal pain, mucus or blood in the stool) and appropriate treatment initiated promptly. (See 'Treatment of immune-mediated toxicity' above.)
Budesonide, an orally administered corticosteroid that is used to treat inflammatory bowel disease, was proposed as a potential way to prevent the immune-related colitis in patients treated with ipilimumab. However, this approach was not beneficial in a randomized phase II trial [11].
Upper gastrointestinal tract involvement has also been reported, including involvement of the esophagus, duodenum, and ileum [21].
Hepatitis — Immune-mediated hepatitis has been seen in 2 to 9 percent of patients treated with ipilimumab [3,7,10]. At least one death due to liver failure has been reported; this was attributed to a delay in the initiation of steroid therapy [10]. The reported incidence of hepatoxicity exceeds 30 percent when ipilimumab is combined with dacarbazine, and the combined used of these agents should be avoided [5].
Hepatic function (transaminase and bilirubin) should be monitored prior to each dose of ipilimumab [14]:
Corticosteroids are the initial treatment for grade 3 or higher hepatic toxicity. Mycophenolate may be useful in patients with persistent severe hepatic toxicity [14]. (See 'Treatment of immune-mediated toxicity' above.)
Dermatitis — Dermatologic side effects are common with ipilimumab therapy and can be manifested by pruritus, rash, vitiligo, and alopecia [22]. In the phase III trial, the incidence of dermatologic adverse events in patients treated with ipilimumab alone was 40 percent; of these, 2.5 percent were more severe (Stevens-Johnson syndrome, toxic epidermal necrolysis, full thickness dermal ulceration) [3,14]. The median time to onset of moderate or severe dermatologic toxicity was three weeks.
Mild to moderate dermatitis (rash, pruritus) can be managed symptomatically. More severe manifestations require discontinuation of ipilimumab and management with corticosteroids. (See 'Treatment of immune-mediated toxicity' above.)
Endocrinopathies — A wide range of autoimmune endocrine side effects have been reported with ipilimumab therapy. Although these are less common than diarrhea and colitis, they have the potential to be serious or fatal.
Hypophysitis and hypopituitarism are uncommon side effects of anti-CTLA-4 immunotherapy [23]. In the phase III trial, nine patients treated with ipilimumab (1.8 percent) had severe or life-threatening hypopituitarism [3,14]. Several of these patients also had other endocrine side effects (hypothyroidism, adrenal insufficiency, or hypogonadism). An additional 12 patients (2.3 percent) had moderate endocrinopathies requiring hormone replacement therapy or other medical intervention. The median time to onset of endocrine symptoms was 11 weeks, but in some cases symptoms did not appear until after completion of the initial four courses of therapy.
Patients should be monitored for clinical signs or symptoms associated with pituitary, thyroid, or adrenal disease [14]. These may be nonspecific, and can include fatigue, headache, mental status changes, abdominal pain, change in bowel habits, or hypotension. Thyroid function and clinical chemistries should be monitored prior to each dose of ipilimumab and as indicated by clinical signs or symptoms. (See "Clinical manifestations of hypopituitarism" and "Diagnosis of hypopituitarism" and "Diagnosis of and screening for hypothyroidism" and "Clinical manifestations of adrenal insufficiency in adults".)
In addition to the endocrine manifestations of hypophysitis, swelling of the pituitary can sometimes be detected on imaging studies and may result in neurologic symptoms including headache or visual abnormalities [22,24]. Swelling of the pituitary must be distinguished from brain metastasis.
Primary thyroid disease can be manifested hyperthyroidism in association with Graves disease or as hypothyroidism secondary to a destructive thyroiditis. Hypothyroidism may also be secondary to hypophysitis, panhypopituitarism, and decreased production of TSH. (See "Diagnosis of and screening for hypothyroidism" and "Overview of the clinical manifestations of hyperthyroidism in adults".)
Treatment of endocrinopathies includes hormone replacement therapy as needed, corticosteroids, and cessation of ipilimumab based upon the severity of the complication. (See 'Treatment of immune-mediated toxicity' above and "Treatment of hypopituitarism" and "Treatment of hypothyroidism" and "Treatment of adrenal insufficiency in adults".)
Other immune-mediated adverse events — Case reports or large series have identified a number of other immune-related adverse events that affect various organ systems:
When rare immune-mediated complications are identified, management should follow the general guidelines for treatment interruption and corticosteroid. (See 'Treatment of immune-mediated toxicity' above.)
OTHER ANTI-CTLA4 ANTIBODIES — Tremelimumab, another monoclonal antibody directed again CTLA-4, showed similar activity compared with ipilimumab in phase I and II clinical studies in previously treated patients [40,41]. This activity provided the basis for a phase III clinical trial in which tremelimumab was compared to chemotherapy (either temozolomide or dacarbazine) in 655 previously untreated patients with metastatic melanoma [42].
Preliminary results of that phase III trial were presented at the American Society of Clinical Oncology (ASCO) meeting in 2008. There was no statistically significant difference in the objective response rate (9.1 versus 10.1 percent for tremelimumab and chemotherapy, respectively) or for overall survival (median 11.8 and 10.7, hazard ratio 1.04, respectively). However, longer follow-up is required to determine whether tremelimumab produces more durable responses than cytotoxic chemotherapy.
SUMMARY AND RECOMMENDATIONS
Choice of therapy — The treatment of metastatic melanoma depends upon multiple factors that include the overall condition of the patient (eg, age and comorbidity), a molecular analysis for the presence of a V600 mutation in the BRAF gene, and the extent of metastatic disease. There are no randomized trials that compare these different approaches and there are no data on the appropriate sequencing of these therapies.
Dose and schedule of ipilimumab
All topics are updated as new information becomes available. Our peer review process typically takes one to six weeks depending on the issue.