Review Article
Medical Progress
Multiple Myeloma
N Engl J Med 1997; 336:1657-1664June 5, 1997DOI: 10.1056/NEJM199706053362307
- Article
Multiple myeloma is a disorder in which malignant plasma cells accumulate in the bone marrow and produce an immunoglobulin, usually monoclonal IgG or IgA. Common complications of overt multiple myeloma include recurrent bacterial infections, anemia, osteolytic lesions, and renal insufficiency. Multiple myeloma is responsible for about 1 percent of all cancer-related deaths in Western countries. Its epidemiologic pattern remains obscure, and its cause is unknown.1
Monoclonal Gammopathy of Undetermined Significance and the Natural History of Multiple Myeloma
A monoclonal gammopathy of undetermined significance is marked by the presence in the serum of monoclonal IgG or IgA without evidence of multiple myeloma. This type of gammopathy is relatively common; it occurs in about 0.15 percent of the general population. Long-term follow-up (for 30 years or more) of patients with this condition has shown that multiple myeloma develops in up to 16 percent, with an annual actuarial risk of 0.8 percent.1,2 The curve describing the risk of multiple myeloma has no plateau, which implies that multiple myeloma can supervene more than 30 years after the initial detection of the gammopathy. Because it is not possible to predict malignant conversion, patients with a monoclonal gammopathy of undetermined significance need long-term follow-up in order to avoid any delay in the diagnosis of overt disease.
Although the frequency with which multiple myeloma appears in patients with monoclonal gammopathy is high, the proportion of all cases of multiple myeloma that develop in this way is unknown.1,2 Some patients who seem to have a monoclonal gammopathy of undetermined significance at the time of their first evaluation actually have indolent multiple myeloma. Such patients have plasma cells with abnormal morphologic features3 that proliferate4 in the bone marrow (increased labeling index),3,5 aneuploidy with chromosomal abnormalities,6 and histologic evidence of abnormal bone remodeling.7 These features may suggest an early diagnosis of multiple myeloma, but it will be important to standardize them if they become part of new diagnostic criteria.
Epidemiologic studies that have identified similar risk factors for monoclonal gammopathy of undetermined significance and multiple myeloma strengthen the link between the two disorders.1,8 The incidence of both conditions increases with the patient's age, is higher among males than among females, and is higher among U.S. blacks than in the general population. Up to 25 percent of patients with Gaucher's disease9 and 15 percent of patients with the acquired immunodeficiency syndrome10 have a monoclonal gammopathy, but in most of these patients there is no evidence of multiple myeloma. The occurrence of monoclonal gammopathy and multiple myeloma in the same families points to the involvement of shared genetic factors in the two disorders.1,8 The strong link between monoclonal gammopathy of undetermined significance and multiple myeloma also supports the two-hit hypothesis of the origin of multiple myeloma, which postulates a first oncogenic event that causes a monoclonal gammopathy and a second that leads to multiple myeloma.11
Clinical Features of Multiple Myeloma
Osteolytic lesions, anemia, renal insufficiency, and recurrent bacterial infections are the most common clinical features of multiple myeloma.12 They have strong diagnostic value if accompanied by more than 10 percent atypical plasma cells in the bone marrow and either a monoclonal immunoglobulin in the serum or light chains in the urine.13 Light chains appear in the serum only if the patient has severe renal failure. Bone lesions, hypercalcemia, and anemia correlate directly with the presence of the total mass of myeloma cells14 and have prognostic value.14-17 All these complications, especially infection and renal insufficiency, are also major causes of death.12 The pathogenesis of these clinical features depends on interactions between myeloma cells and the microenvironment of the bone marrow by means of cell-to-cell contact, adhesion molecules, and cytokines18 or on the direct effects of circulating monoclonal immunoglobulins or light chains.19
The clinical presentation of multiple myeloma has tended to shift from overt symptoms to indolent or localized disease. Of the patients with overt multiple myeloma who were referred to one center, 58 percent had an earlier plasma-cell disorder, such as monoclonal gammopathy of undetermined significance, smoldering myeloma (that is, a monoclonal gammopathy with atypical plasma cells in the bone marrow, but without anemia, bone lesions, or renal failure), solitary myeloma, or extramedullary plasmocytoma.20 Recent studies have shown that magnetic resonance imaging (MRI) can detect involvement of the vertebral marrow in 50 percent of patients with indolent myeloma (defined as asymptomatic multiple myeloma with fewer than four osteolytic lesions and normal renal function).21,22 Moreover, one third of patients considered to have a solitary plasmocytoma according to standard criteria have bone marrow abnormalities consistent with multiple myeloma on MRI.23
The Biology of Normal and Malignant Plasma Cells
A small number of long-lived plasma cells in the bone marrow (less than 1 percent of mononuclear cells) produce most of the IgG and IgA in the serum. The daily production of immunoglobulin by these cells can exceed 1 ng per cell. These well-differentiated cells do not divide and have a characteristic phenotype: CD38bright, syndecan-1bright, CD19+, and CD56weak/-. Their precursors are slowly proliferating plasmablasts, which migrate to the marrow from lymph nodes after stimulation by antigens and cytokines from helper T cells in the germinal centers. These events in germinal centers initiate somatic mutations of the immunoglobulin genes of B cells and a switch from the production of IgM to the production of IgG or IgA. After the activated B cells enter the bone marrow, they stop proliferating and differentiate into plasma cells, under the influence of adhesion molecules and factors such as interleukin-6. Plasma cells die by apoptosis after several weeks or months, but what initiates the process is unclear.24
In contrast to normal plasma cells, myeloma cells are often immature and may have the appearance of plasmablasts (Figure 1Figure 1
A Cluster of Malignant Plasmablasts.).25 They usually are CD19- CD56bright,26 CD38, and syndecan-1, and they produce very low amounts of immunoglobulins (a few picograms per cell per day).27 In almost all patients, the myeloma cells are aneuploid (more often hyperdiploid than hypodiploid),28 and their chromosomes have many numerical and structural abnormalities, mainly on chromosomes 13 (13q-) and 14 (14q+).29 These genetic abnormalities may prevent the differentiation and normal death of the myeloma cells, which continue to proliferate and accumulate in the bone marrow. The morphologic immaturity (cells taking the form of plasmablasts),30,31 hypodiploidy,32 and the 13q- and 14q+ abnormalities33 correlate with the resistance to treatment and short survival characteristic of aggressive disease.The somatic mutations of the immunoglobulin genes of myeloma cells34 indicate that the putative myeloma-cell precursors are stimulated by antigens and are either memory B cells or migrating plasmablasts. The stability of the mutations35 and of the antigenic properties (the idiotype) of the myeloma protein during the course of the disease has clinical implications. The mutations, which are molecular signatures of the neoplastic clone, might be useful for detecting residual myeloma cells after chemotherapy. Vaccination with the myeloma idiotype of a monoclonal immunoglobulin is a potential means of immunotherapy.
Multiple Myeloma as a Multistep Process
Myeloma cells proliferate slowly in the marrow. Less than 1 percent of them divide at any one time,36 and they do not differentiate completely. The cause of this failure to differentiate is unknown, but translocations between 14q32 and its chromosome partners (chromosomes 11, 6, 16, 9, 18, and 8)29,33 and deregulation of the c-myc oncogene37 may be important. The growth fraction of the tumor is high (more than 20 percent) in relapses in bone marrow, but especially so in relapses outside the bone marrow.36 Point mutations of the N-ras and K-ras oncogenes have been found in relapses in marrow,38 and point mutations of p53 have been identified in extramedullary relapses of myeloma39 (Table 1Table 1
Three Phases of Disease Progression in Multiple Myeloma.). Cytologic25,30 and phenotypic40 changes have also been associated with both these types of relapses (Table 1). Although p53 mutations are rarely seen at the time of diagnosis, N-ras and K-ras mutations are apparent in up to 15 percent of patients given a new diagnosis of multiple myeloma. K-ras mutations are associated with shorter survival.41 Multiple myeloma is usually thought to be confined to the bone marrow, but recent studies have noted circulating myeloma cells in many patients.42 The absolute number of these cells correlates with disease activity and predicts the progression of disease in smoldering multiple myeloma. Circulating myeloma cells may disseminate the tumor within the bone marrow and elsewhere.
Interleukin-6 and the Bone Marrow Microenvironment
Interleukin-6 is essential for the survival and growth of myeloma cells,43,44 which express specific receptors for this cytokine. The interleukin-6 receptor has two polypeptide components: the α chain (composed of the glycoprotein subunit gp80, or interleukin-6 receptor α) and the β chain, a transducer element (gp130). Interleukin-6 belongs to a family containing five other cytokines that use gp130 as a transducer: oncostatin M, leukemia inhibitory factor, interleukin-11, ciliary neurotropic factor, and cardiotrophin 1. Interleukin-6 was initially found to be a growth factor for myeloma cells,43,44 but recently it was also shown to promote the survival of myeloma cells by preventing spontaneous or dexamethasone-induced apoptosis.45 These data from in vitro studies suggest that interleukin-6 promotes both tumor growth and resistance to dexamethasone in vivo. The beneficial effects of therapy with murine anti–interleukin-6 monoclonal antibodies in some patients with advanced multiple myeloma also support this supposition.46
There is increasing evidence that interleukin-6 is not an autocrine growth factor,43 but the product of other cells in the microenvironment of the marrow.44 Indeed, myeloma cells can stimulate stromal cells and bone cells to release large amounts of interleukin-6.47 Various membrane proteins on myeloma cells (and on their normal neighbors in the marrow), in addition to soluble factors produced by normal cells in the microenvironment, help induce the production of interleukin-6.47 The increased levels of interleukin-6 in the serum of patients with multiple myeloma can be explained by the overproduction of interleukin-6 in the marrow. Myeloma cells shed the soluble form of interleukin-6 receptor α, which can amplify the response of myeloma cells to interleukin-6.48 Interleukin-6 receptor α is present in high amounts in the serum of patients with myeloma, especially those with a poor prognosis. The interleukin-6 system also has a role in the pathogenesis of bone lesions in multiple myeloma.49 Interleukin-6, soluble interleukin-6 receptor α, and interleukin-1β activate osteoclasts in the vicinity of myeloma cells and thus provoke bone resorption.
Therapy
Conventional-Dose Chemotherapy
Melphalan, cyclophosphamide, and glucocorticoids are the most effective drugs against multiple myeloma; the classic combination of melphalan and prednisone is still the standard treatment for most patients.50 Combinations of other drugs, including vinca alkaloids, nitrosoureas, and anthracyclines, are active against myeloma but are no more effective than melphalan and prednisone.50 Results with novel agents like purine analogues or taxane derivatives have not been promising. The regimen of vincristine, doxorubicin, and dexamethasone (VAD) — or a similar combination, with high-dose methylprednisolone substituted for high-dose dexamethasone (VAMP) — which is often used in patients with newly diagnosed disease, has not prolonged survival more than other regimens in a randomized clinical trial; its main advantage is the rapid induction of remission.50
The value of agents that inhibit multidrug resistance in vitro, such as verapamil and cyclosporine, has been evaluated in patients with multiple myeloma resistant to VAD.51,52 However, because expression of the protein for multidrug resistance is related to a history of chemotherapy53 and because the toxicity of these drugs is substantial, they offer little promise in patients with newly diagnosed disease. The results of treatment with high doses of glucocorticoids (e.g., dexamethasone) alone in patients with relapses or with refractory disease and in previously untreated patients50 are inferior to those associated with VAD.
High-Dose Therapy
The lack of progress with conventional chemotherapy has heightened interest in high-dose therapy. Treatment with melphalan in high doses (140 mg per square meter of body-surface area, given intravenously without hematopoietic support) can induce complete remissions in 20 to 30 percent of patients (including disappearance of the M component),54-56 but it causes severe and sometimes irreversible myelosuppression. The rate of death due to the toxicity of this treatment is approximately 10 percent in patients with newly diagnosed disease55,56 and more than 20 percent in previously treated patients.54 The addition of granulocyte–macrophage colony-stimulating factor (GM-CSF) or granulocyte colony-stimulating factor (G-CSF) to the regimen reduces the duration of neutropenia but does not significantly reduce morbidity or mortality due to infection and does not eliminate the risk of protracted aplasia.57,58
Transplantation of autologous hematopoietic stem cells (obtained from bone marrow or blood) accelerates the restoration of hematopoiesis after the administration of high-dose melphalan and allows for a combination of intensive chemotherapy and total-body irradiation or for the use of higher doses of melphalan (200 mg per square meter).59 Autologous stem-cell transplantation may be a useful form of salvage therapy for patients whose disease is refractory to initial standard chemotherapy and for patients in relapse with chemosensitive myeloma, but it has limited value for patients in relapse with resistant myeloma.60
Uncontrolled studies of patients with newly diagnosed disease have shown that the combination of conventional induction therapy and high-dose therapy followed by autologous stem-cell transplantation produces a 30 to 50 percent rate of complete remission61,62 (defined as the disappearance of the M component as determined by standard electrophoresis) and prolongs survival.59,61-63 However, all these studies were marked by selection bias. The Intergroupe Français du Myélome has recently reported the results of an intention-to-treat analysis of data from 200 patients 65 years of age or less who were randomly assigned at diagnosis either to conventional multiagent chemotherapy or to intensive therapy with autologous bone-marrow transplantation.64 The rates of remission, event-free survival, and overall survival were significantly better in the intensive-therapy group. The patients who received conventional chemotherapy had results similar to those in the literature.
This trial suggests that intensive therapy with autologous hematopoietic support represents a significant improvement over conventional therapy and may be the treatment of choice for patients up to 65 years of age. However, in this study the intensive therapy was actually completed in only 58 percent of the patients over the age of 60. The feasibility of intensive therapy in older patients remains a critical issue because the median age of patients at diagnosis is about 65 years and candidates for the treatment must have a good performance status and normal renal function. For many patients, conventional chemotherapy is therefore the only possibility.
Currently, hematopoietic stem cells from peripheral blood are preferred for transplantation because they restore hematopoiesis more rapidly than do bone marrow cells.61 The administration of growth factors after transplantation and the use of hematopoietic-cell progenitors collected from blood after the patient has been given G-CSF or GM-CSF appear to further accelerate hematologic reconstitution.65,66 Autologous stem-cell transplantation is now a safe procedure (with a rate of death due to toxic effects of 1 to 2 percent in patients with newly diagnosed disease). However, contamination of the autologous graft by myeloma cells remains a concern. Studies with gene-marking techniques suggest that tumor cells in the graft contribute to relapse, although purging marrow in vitro with cyclophosphamide derivatives or with monoclonal antibodies still does not adequately restore hematopoiesis.67,68 The transplantation of purified CD34+ progenitors is a promising alternative to the purging technique, because this method can reduce the number of contaminating tumor cells by up to 99.99 percent.66,69 Nevertheless, polymerase-chain-reaction assays for clonally unique immunoglobulin gene mutations have detected myeloma cells in such purified CD34+ cell fractions,66,69 and an additional purging may be necessary to obtain grafts free of myeloma cells.70 The clinical effect of these expensive procedures has not yet been evaluated.
The lack of a plateau in the survival curves plotted with data from trials with adequate follow-up implies that curing multiple myeloma with a single course of intensive therapy is unlikely. Because patients in whom the paraprotein level decreases by at least 90 percent have the longest remissions and survival,64 future studies should aim to increase the rate of complete remission. To attain this objective, two successive courses of intensive therapy56 and tandem transplantations of peripheral-blood progenitors71,72 have been tried, but the effect of this aggressive strategy on overall survival is still unknown.
In patients 50 years of age or younger, allogeneic transplantation of bone marrow from an HLA-identical sibling yields encouraging results if undertaken early in the course of disease.73 Although the rate of death due to toxicity is high and late relapses occur, approximately one third of the patients who have a complete remission after transplantation remain free of disease six years later. As a result of the antitumor effects of the graft, allogeneic transplantation is possibly the only genuinely curative therapy in myeloma. The recent report of a patient with refractory myeloma who achieved complete remission after the infusion of peripheral-blood mononuclear cells from a donor is a further demonstration of this graft-versus-myeloma effect.74
Interferon Alfa
Therapy against multiple myeloma with interferon alfa is still controversial 15 years after its introduction. Pilot studies found evidence of remissions in refractory or relapsing multiple myeloma, but interferon alfa was not shown to be superior to conventional chemotherapy in previously untreated patients.75 Currently, interferon alfa is used as maintenance therapy for patients who have a response to initial treatment or, in combination with chemotherapy, as induction therapy. The prolonged remissions obtained with interferon alfa in an Italian multicenter study76 prompted a number of prospective, randomized studies.77-81 All these trials compared moderate doses of interferon alfa (2 to 3 megaunits per square meter, given three times a week) with a regimen of observation alone after conventional induction chemotherapy. Of the trials, two found no significant advantage associated with maintenance therapy with interferon alfa,77,80 but in four others, the median duration of remission was 5 to 12 months longer than in the control group.76,78,79,81 However, for reasons that are unclear, the lengthened remissions were not associated with significantly longer survival. Prolongation of remission without prolongation of survival was also observed in a trial conducted by the Nordic Myeloma Study Group, in which patients were randomly assigned to receive interferon alfa or not to receive this agent through induction treatment, plateau phase, and relapse.82 Since treatment with interferon alfa can impair the patient's quality of life, the clinical benefit of prolonging remission is uncertain.83
Interferon alfa has also been given to patients after high-dose therapy on the assumption that it may be more effective in patients with only minimal residual disease. In one randomized study, the median period of progression-free survival was significantly longer for patients given interferon alfa than for those patients who were not.84
Eight randomized studies have investigated the effects of varying doses of interferon alfa combined with induction chemotherapy.81,82,85-90 In one study from Sweden,85 the rates of remission and survival were significantly higher among patients given natural interferon alfa, but the benefit was restricted to patients with IgA and Bence Jones myeloma and patients with stage II disease. Except in one small study,88 the rates of remission and survival were not improved by therapy with recombinant interferon alfa. Pilot studies have had encouraging results with the combination of interferon alfa and high-dose dexamethasone.77,91
New Supportive Therapies
Bisphosphonates
Bisphosphonates, which are potent inhibitors of bone resorption, have been widely used in multiple myeloma, primarily for the treatment of hypercalcemia. They may also contribute to the long-term control of bone disease; three multicenter, placebo-controlled studies have investigated this possibility (Table 2Table 2
Placebo-Controlled Trials of Bisphosphonates in Patients with Multiple Myeloma.).92-94 Studies of etidronate and clodronate did not find any benefits associated with the drugs, but the results with pamidronate appear promising. Pamidronate reduced the incidence of skeletal events (pathologic fractures, the need for irradiation or surgery of bone, and spinal cord compression), prevented hypercalcemia, alleviated bone pain, and improved the patient's quality of life.94 The recent availability of more potent bisphosphonates will open new avenues for the treatment of bone disease in multiple myeloma.Erythropoietin
Phase 1–2 clinical trials have had encouraging results with recombinant human erythropoietin for the treatment of the anemia of multiple myeloma; these data suggest a correlation between the pretreatment serum level of erythropoietin and the clinical response. Two recent randomized studies have confirmed that recombinant-erythropoietin therapy is safe and can decrease the need for transfusion in selected patients.95,96 In both studies the likelihood of response was highest in patients with erythropoietin levels that were inadequately low for the degree of anemia.
Future Approaches
Interleukin-2, interleukin-4, interferon gamma, and tretinoin have been investigated in pilot studies.75 Either the agents had no observed significant benefit or the benefit was not yet substantial enough for the drugs to be recommended, even in patients with advanced multiple myeloma. Treatment of advanced multiple myeloma with murine anti–interleukin-6 monoclonal antibodies has produced some effect but no lasting benefit.97 Trials with chimeric human–murine anti–interleukin-6 monoclonal antibodies, anti–interleukin-6–receptor antibodies, and new interleukin-6 inhibitors are under way. The value of immunotherapy has not yet been extensively evaluated in multiple myeloma. The idiotype (i.e., the unique antigenic structure) of the monoclonal immunoglobulin in an individual patient could be a tumor-specific antigen. T cells that recognize the idiotypes of the patient's myeloma protein are present in multiple myeloma,98 but functional abnormalities of these T cells may explain why they are ineffective against the tumor in vivo.99 In one patient, idiotype-specific immunity was transferred from a bone marrow donor after the donor was immunized with the purified IgG of the patient.100 Two years after transplantation, the patient remained well with a minimal M component. Immunotherapy is also being evaluated in patients who have had autologous transplantation with the aim of eradicating any residual disease.
Supported by the Ligue Contre le Cancer and the Association pour la Recherche sur le Cancer.
We are indebted to Mrs. C. Avet Loiseau for typing the manuscript and to Mrs. L. Bataille-Zagury for editing assistance.
Source Information
From the Laboratory of Hematology, Institute of Biology (R.B.), and the Department of Clinical Oncology and Hematology (J.-L.H.), University Hospital, Nantes, France.
Address reprint requests to Dr. Bataille at the Laboratoire d'Hématologie, Institut de Biologie, 9, Quai Moncousu, 44035 Nantes CEDEX 01, France.
- References
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