Division of Hematology, Department of Internal Medicine, Mayo Clinic and Mayo Foundation, Rochester, Minnesota, USA
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1 The Oncologist Fundamentals of Cancer Medicine Waldenström s Macroglobulinemia MORIE A. GERTZ, RAFAEL FONSECA, S. VINCENT RAJKUMAR Division of Hematology, Department of Internal Medicine, Mayo Clinic and Mayo Foundation, Rochester, Minnesota, USA Key Words. Waldenström s macroglobulinemia Hyperviscosity Lymphoma Monoclonal gammopathy Chlorambucil Fludarabine ABSTRACT Waldenström s macroglobulinemia is a low-grade lymphoplasmacytic lymphoma. It has an overall incidence of 2.5/million/year. The median age at diagnosis is 63 years. The clinical manifestations are hepatomegaly (20%), splenomegaly (15%), and lymphadenopathy (15%). The most common symptom is fatigue related to a normochromic, normocytic anemia, and the median hemoglobin value at diagnosis is 10 gm/dl. All patients with Waldenström s macroglobulinemia have a circulating tumor marker, the monoclonal IgM protein. Occasionally high levels of the IgM monoclonal protein INTRODUCTION In 1944, Jan Waldenström described two patients with hepatosplenomegaly, anemia, oronasal bleeding, and a peculiar protein in the serum. Dr. Waldenström noticed that most normal serum globulin sedimented with a coefficient of 7S. In his patients the preponderance of serum globulin had a sedimentation coefficient of 19S. His initial description contains most of the salient features of the low-grade lymphoplasmacytic disorder that today carries his name. This is remarkable as Waldenström s description appeared before the development of paper electrophoresis, so the concept of a monoclonal serum peak did not exist. Immunoelectrophoresis classifying serum heavy chains into G, A, and M was not generally available. Not until 1937 did Teselius describe the separation of serum globulins into α, β, and γ, and the concept of immunoglobulins was not proposed until the late 1950s. can produce a hyperviscosity syndrome manifested by oronasal bleeding. Occasionally retinal hemorrhage or serious neurologic complications, such as somnolence or coma, may occur. The most important prognostic factors are hemoglobin, age, weight loss, and a cryoglobulin. Therapy has included alkylating agents, particularly chlorambucil, purine nucleoside analogs such as fludarabine or cladribine, and most recently the use of rituximab. The median survival of symptomatic patients is 65 months. Patients without symptoms should not be treated. The Oncologist 2000;5:63-67 CLINICAL ASPECTS OF WALDENSTRÖM S MACROGLOBULINEMIA Presence of Monoclonal Proteins Monoclonal proteins are found in population-based screening studies in 1% of patients over the age of 50 years and in 3% to 4% of patients over the age of 70 years. Figure 1 illustrates the distribution of monoclonal proteins found in samples studied in the special protein laboratory of the Mayo Clinic. The IgM monoclonal proteins are second only to IgG proteins in frequency, and occur more often than IgA monoclonal proteins. Diseases associated with IgM monoclonal proteins are listed in Figure 2; IgM monoclonal gammopathy of undetermined significance (MGUS) is the most common and Waldenström s macroglobulinemia, the next most common. IgM monoclonal protein may also be detected in patients with malignant lymphoma, lymphoproliferative disorders, Correspondence: Morie A. Gertz, MD, Division of Hematology, Department of Internal Medicine, Mayo Clinic, Rochester, MN 55905, USA. Telephone: ; Fax: ; gertz.morie@mayo.edu Accepted for publication January 13, AlphaMed Press /2000/$5.00/0 The Oncologist 2000;5:
2 64 Waldenström s Macroglobulinemia Figure 1. Incidence of IgM monoclonal gammopathies. Figure 2. Diseases associated with IgM monoclonal proteins. chronic lymphocytic leukemia (CLL), primary systemic amyloidosis, cryoglobulinemia, and demyelinating neuropathies. Timing of Therapy Not all patients with an IgM monoclonal protein in the serum and a lymphoplasmacytic infiltrate in the bone marrow require immediate therapy. Some patients with IgM monoclonal proteins will not have anemia, symptoms of hyperviscosity, or pulmonary or neurologic problems and can be safely observed. Since the development of Waldenström s macroglobulinemia is an indolent process, patients can have an IgM monoclonal gammopathy observed for years and not require therapeutic intervention. The first critical decision to make is whether the patient with an IgM monoclonal protein or macroglobulinemia has sufficient symptoms to warrant therapy. Even patients who have IgM values >3,000 mg/dl may be asymptomatic, have a normal hemoglobin value, and have no clinically important increase in the serum viscosity level. For them, observation remains an appropriate option. The point at which MGUS evolves into Waldenström s macroglobulinemia remains ill-defined. Certainly patients who develop a progressive normochromic, normocytic anemia due to lymphoplasmacytic marrow infiltration no longer have MGUS. The distinction between MGUS and Waldenström s macroglobulinemia is a clinical one, however; patients with MGUS have a normal hemoglobin value and no increase in circulating lymphocytes in the blood, palpable lymphadenopathy, compatible amyloidosis syndrome, or symptoms of hyperviscosity. Waldenström s macroglobulinemia with diffuse marrow infiltration by lymphocytes with plasmacytic morphology can strongly mimic CLL. Anemia is the most common indication for therapy. Historically Waldenström s macroglobulinemia has been defined as an M protein of >3 g/dl. Subsequently we have found little difference in the clinical course and survival between those patients who have an M protein >3 g/dl and those who have an M protein ranging from 1 to 3 g/dl. Therefore, the distinction is arbitrary and Waldenström s macroglobulinemia and a lymphoproliferative disorder with a circulating monoclonal IgM protein can be considered a single entity. Disease Onset and Characterization The median age of onset of Waldenström s macroglobulinemia is 63 years. Five percent of patients have an associated peripheral neuropathy. Hepatomegaly is seen in 20%, splenomegaly in 15%, and enlarged lymph glands in approximately 15% of patients. The median serum monoclonal protein level for symptomatic Waldenström s macroglobulinemia is 4 g/dl. The most common laboratory finding in symptomatic Waldenström s macroglobulinemia is anemia, with a median hemoglobin value of approximately 10 g/dl. As in most other monoclonal gammopathies, the κ:λ ratio in Waldenström s macroglobulinemia is approximately 3:1, and contrary to the notion that a monoclonal light chain infrequently appears in urine, a light chain appears in the urine of nearly 80% of patients with macroglobulinemia [1]. Waldenström s macroglobulinemia, unlike CLL or nodular lymphoma, has three important distinguishing features: pulmonary involvement, peripheral neuropathy, and hyperviscosity syndrome. Pulmonary involvement in Waldenström s macroglobulinemia can occur in the absence of hilar or mediastinal lymphadenopathy. Biopsy demonstrates diffuse infiltration of pulmonary parenchyma with lymphoplasmacytoid cells and will stain for the monoclonal IgM protein [2, 3]. In most cases of peripheral neuropathy associated with Waldenström s macroglobulinemia, the IgM monoclonal
3 Gertz, Fonseca, Rajkumar 65 protein has antimyelin-associated glycoprotein activity, leading to binding to the myelin sheath of the peripheral nerve and a demyelinating peripheral neuropathy [4]. In one study peripheral neuropathy was found in 12 of 26 patients with macroglobulinemia, and antimyelin-associated glycoprotein activity was found in six of those 12 patients. Sural nerve biopsy showed demyelination and IgM deposits in the myelin sheath [5]. Disease Prevalence In 11 population-based registries in the United States, the age-adjusted rates were 3.4 and 1.7 per million among men and women, respectively. Rates increased sharply with age: 0.1 per million at age <45 years and 36.3 per million at age 75+ years. These rates are comparable to those for hairy-cell leukemia, and do not appear to be increasing. The rates are clearly higher in Caucasians compared with African-Americans [6]. HYPERVISCOSITY SYNDROME Hyperviscosity syndrome is associated with disorders of monoclonal immunoglobulins. When large, positively charged IgM molecules are present in excess, they bind electrostatically to red cells, causing aggregation and rouleaux, and thereby increase the blood viscosity. As the protein concentration in the serum increases, the viscosity increases exponentially. In 35 patients with Waldenström s macroglobulinemia, most symptomatic patients had whole blood viscosity levels >8 cp, and hyperviscosity was reported in 8% to 39% of patients. The most common symptoms of Waldenström s macroglobulinemia are oronasal bleeding, dizziness, and visual disturbances due to retinal bleeding (Fig. 3). The level of serum viscosity has not been demonstrated to have an effect on survival time. Serum viscosity levels (relative to water) >6 most commonly occur with IgM values >5 g/dl. Small reductions in the circulating M protein with plasma exchange can dramatically reduce the viscosity and lead to resolution of symptoms (Table 1). Relative serum viscosity levels between two and four are rarely associated with symptoms, but occasionally, a patient with a viscosity between four and five will have symptoms. Most symptomatic patients have a viscosity between five and eight, and virtually all patients with viscosities >8 will have symptoms. Of 51 patients with Waldenström s macroglobulinemia, serum viscosity was found to be >4 in 15 patients; five of these 15 patients had no symptoms related to the increased viscosity. Nine patients had bleeding (manifested by epistaxis in seven), three patients had gingival bleeding, and three patients had blurred vision. All patients had concentrations of M protein 4.3 g/dl. Screening for hyperviscosity in asymptomatic patients with IgM peaks <4 g is unnecessary. The relationship Table 1. Clinical manifestations of hyperviscosity Mucosal hemorrhage Gingival Epistaxis Gastrointestinal bleeding Postsurgical bleeding Visual abnormalities Blurring or visual loss Retinal vein thrombosis Retinal hemorrhage and exudates Papilledema Neurological Headache Vertigo Deafness Syncope Ataxia Diplopia Somnolence or coma Cerebral hemorrhage Seizures Chorea Cardiac Heart failure (high output versus increased afterload) between viscosity and symptoms is unclear, but in our experience, a single plasma exchange produces a marked clinical benefit [7]. The efficacy of plasmapheresis was studied in four patients with macroglobulinemia who underwent 22 plasma exchanges. Monoclonal protein concentrations after Figure 3. Retinal hemorrhages due to hyperviscosity. Figure 4. Bone marrow aspirate in a patient with Waldenström s (Wright s stain 100).
4 66 Waldenström s Macroglobulinemia plasma exchange decreased an average of 35%, and plasma viscosity decreased from 5 to 2.1 [8]. HISTOPATHOLOGY Of 137 patients with Waldenström s macroglobulinemia, bone marrow involvement was present in 80% of patients on a first marrow biopsy, and 18% of patients were positive with subsequent biopsy (Fig. 4). Using flow cytometry an abnormal clone of B cells is routinely found in the peripheral blood and bone marrow. Waldenström cells express surface immunoglobulin and strongly express CD19, CD20, and CD22 cells. These cells weakly express cytoplasmic immunoglobulin, CD10, and CD38. The flow characteristics of the cells can help distinguish Waldenström s macroglobulinemia from multiple myeloma. Multiple myeloma cells strongly express CD38 and cytoplasmic immunoglobulin. Flow is also useful in separating Waldenström s from CLL, since patients with CLL strongly express CD5 and CD21 cells. The patterns of bone marrow infiltration can be diffuse, nodular interstitial, mixed paratrabecular nodular, and paratrabecular. These histologic features apparently do not correlate significantly with survival [9]. PROGNOSIS Gobbi et al. [10] have established a prognostic index for macroglobulinemia using 144 patients with clinically overt macroglobulinemia. All patients were treated uniformly with chlorambucil. On univariate analysis the most important parameters were age > or <70 years, platelet count > or < /l, presence or absence of red cells in the urine, hemoglobin > or <9 g/dl, sedimentation rate 110 mm, presence or absence of a cryoglobulinemia, and weight loss. On a Cox multivariate analysis, hemoglobin, age, weight loss, and cryoglobulinemia independently affected survival. A clearcut survival discriminant was reached using an index of 0 or 1 factors versus 2 of these four prognosticators [10]. Bone marrow pathology and overall survival show a correlation. Patients with lymphoplasmacytoid morphology had a median survival of 74 months; those with lymphoplasmacytic morphology had a median survival of 25 months; and patients with polymorphous change had a median survival of 12 months. The percentage of lymphocytic infiltration in the bone marrow also correlated with survival: <20% infiltration was associated with a >50-month median survival, 20% to 50%, a 40-month median survival, and >50% infiltration, a 24-month median survival. THERAPY Although durable responses have been reported after splenectomy [11] and treatment with α2 interferon [12], the mainstay of treatment of Waldenström s macroglobulinemia is systemic chemotherapy. The Mayo Clinic conducted a study of chlorambucil therapy for the treatment of Waldenström s macroglobulinemia using the M component and the hemoglobin value as response endpoints. Forty-six patients were treated, and 36 (79%) had an objective response. Oral daily chlorambucil and intermittent pulse chlorambucil were similar in terms of response rate or survival. Median duration of survival was 5.4 years. Patients needed >6 months of therapy because responses were slow. An unexpectedly high incidence of myelodysplastic syndromes (3 of 46 patients) was seen. Vincristine, BCNU, melphalan, cyclophosphamide, and prednisone have also been used in the treatment of Waldenström s macroglobulinemia with a response rate of 81%. This response rate does not appear superior to that seen with the single alkylating agent chlorambucil [13]. Researchers at M.D. Anderson Cancer Center (Houston, Texas) have worked extensively using purine nucleoside analogs for the management of Waldenström s macroglobulinemia. Fludarabine produced a response rate of 36% and 31% in patients resistant to prior therapies. Fludarabine was found to be an effective salvage regimen [14]. In a study from Italy, the partial response rate was 41% among 12 patients with Waldenström s macroglobulinemia resistant to alkylating agent-based treatment [15]. In a multicenter study using fludarabine in previously untreated patients with Waldenström s macroglobulinemia, the response rate was 79%, median duration of response was 2.5 years, and treatment-related mortality was 5% [16]. (The treatment-related mortality with chlorambucil is nearly zero.) Cladribine has been used to treat Waldenström s macroglobulinemia. Of 29 symptomatic patients with macroglobulinemia after two courses of cladribine, 59% of patients responded: 100% of newly diagnosed patients and 40% of those who had failed previous therapy [17]. In a follow-up study by the same authors [18] using two courses of cladribine, the response rate was 85%, including three complete responses. At a median follow-up of 13 months, five patients had relapsed and subsequently responded to retreatment. A comprehensive review of this information has recently been published [19]. Cladribine does not have to be administered by continuous i.v. infusion; bolus administration is also effective, producing complete responses in 5% and partial responses of 50% with a median duration of 28 months [20]. The cells of macroglobulinemia strongly express CD20, so it is reasonable to expect rituximab (Rituxan, a monoclonal antibody which selectively depletes normal and malignant CD20 + pre-b and mature B cells) to be an active agent in treatment. Seven patients with Waldenström s macroglobulinemia previously treated with alkylators received rituximab. Four had also received fludarabine. Responses were seen in 57% of patients with a median progression-free survival of eight months. The Eastern
5 Gertz, Fonseca, Rajkumar 67 Cooperative Oncology Group is planning a study of rituximab in patients with untreated and previously treated Waldenström s macroglobulinemia. LATE COMPLICATIONS The two major late complications of Waldenström s macroglobulinemia are Richter s transformation and myelodysplasia related to therapy. As in all low-grade lymphomas, treated or untreated, a large-cell lymphoma or immunoblastic sarcoma can develop [21, 22]. Since alkylating agents have been a mainstay of therapy for macroglobulinemia for many years, the development of myelodysplasia or acute leukemia is well reported. Most REFERENCES 1 Kyle RA, Garton JP. The spectrum of IgM monoclonal gammopathy in 430 cases. Mayo Clin Proc 1987;62: Kobayashi H, Ii K, Hizawa K et al. Two cases of pulmonary Waldenström s macroglobulinemia. Chest 1985;88: Fadil A, Taylor DE. The lung and Waldenström s macroglobulinemia. South Med J 1998;91: Vital C, Deminiere C, Bourgouin B et al. Waldenström s macroglobulinemia and peripheral neuropathy: deposition of M-component and kappa light chain in the endoneurium. Neurology 1985;35: Nobile-Orazio E, Marmiroli P, Baldini L et al. Peripheral neuropathy in macroglobulinemia: incidence and antigen-specificity of M proteins. Neurology 1987;37: Groves FD, Travis LB, Devesa SS et al. Waldenström s macroglobulinemia: incidence patterns in the United States, Cancer 1998;82: Gertz MA, Kyle RA. Hyperviscosity syndrome. J Intensive Care Med 1995;10: Reinhart WH, Lutolf O, Nydegger UR et al. Plasmapheresis for hyperviscosity syndrome in macroglobulinemia Waldenström and multiple myeloma: influence on blood rheology and the microcirculation. J Lab Clin Med 1992;119: Andriko JA, Aguilera NS, Chu WS et al. Waldenström s macroglobulinemia: a clinicopathologic study of 22 cases. Cancer 1997;80: Gobbi PG, Bettini R, Montecucco C et al. Study of prognosis in Waldenström s macroglobulinemia: a proposal for a simple binary classification with clinical and investigational utility. Blood 1994;83: Humphrey JS, Conley CL. Durable complete remission of macroglobulinemia after splenectomy: a report of two cases and review of the literature. Am J Hematol 1995;48: Rotoli B, De Renzo A, Frigeri F et al. A phase II trial on alpha-interferon (alpha IFN) effect in patients with monoclonal IgM gammopathy. Leuk Lymphoma 1994;13: patients eventually die as a consequence of chemotherapy resistance. SUMMARY Waldenström s macroglobulinemia is a low-grade lymphoproliferative disorder that is characterized by normochromic, normocytic anemia and lymphoplasmacytic marrow infiltration. A monoclonal IgM protein is seen in all patients with Waldenström s macroglobulinemia and can produce hyperviscosity in a few. Therapy has included alkylating agents, both single and in combination, purine nucleoside analogs, and rituximab on an investigational basis. 13 Case DC Jr, Ervin TJ, Boyd MA et al. Waldenström s macroglobulinemia: long-term results with the M-2 protocol. Cancer Invest 1991;9: Dimopoulos MA, O Brien S, Kantarjian H et al. Fludarabine therapy in Waldenström s macroglobulinemia. Am J Med 1993;95: Zinzani PL, Gherlinzoni F, Bendandi M et al. Fludarabine treatment in resistant Waldenström s macroglobulinemia. Eur J Haematol 1995;54: Foran JM, Rohatiner AZ, Coiffier B et al. Multicenter phase II study of fludarabine phosphate for patients with newly diagnosed lymphoplasmacytoid lymphoma, Waldenström s macroglobulinemia, and mantle-cell lymphoma. J Clin Oncol 1999;17: Dimopoulos MA, Kantarjian H, Estey E et al. Treatment of Waldenström macroglobulinemia with 2-chlorodeoxyadenosine. Ann Intern Med 1993;118: Dimopoulos MA, Kantarjian H, Weber D et al. Primary therapy of Waldenström s macroglobulinemia with 2-chlorodeoxyadenosine. J Clin Oncol 1994;12: O Brien S, Kantarjian H, Keating MJ. Purine analogs in chronic lymphocytic leukemia and Waldenström s macroglobulinemia. Ann Oncol 1996;7:S27-S Liu ES, Burian C, Miller WE et al. Bolus administration of cladribine in the treatment of Waldenström macroglobulinaemia. Br J Haematol 1998;103: Abe M, Takahashi K, Mori N et al. Waldenström s macroglobulinemia terminating in immunoblastic sarcoma. A case report. Cancer 1982;49: Choi YJ, Yeh G, Reiner L et al. Immunoblastic sarcoma following Waldenström s macroglobulinemia. Am J Clin Pathol 1979;71:
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