Indolent B-Cell Non-Hodgkin Lymphoma
Indolent B-cell non-Hodgkin lymphoma (NHL) includes the following subtypes:
- Follicular lymphoma (grades 1–3a).
- Lymphoplasmacytic lymphoma (Waldenström macroglobulinemia).
- Marginal zone lymphoma.
Follicular Lymphoma (Grades 1–3a)
Follicular lymphoma makes up 20% of all NHL and as many as 70% of the indolent lymphomas reported in American and European clinical trials.[1,2,3] Most patients with follicular lymphoma are aged 50 years and older and present with widespread disease at diagnosis. Nodal involvement is most common and is often accompanied by splenic and bone marrow disease. Rearrangement of the BCL2 gene is present in more than 90% of patients with follicular lymphoma. Overexpression of the BCL2 protein is associated with the inability to eradicate the lymphoma by inhibiting apoptosis.[4]
Prognosis
Follicular lymphoma is designated as indolent because median survival ranges from 8 to 15 years, even in advanced stages.[5,6,7] Patients with advanced-stage follicular lymphoma are not cured with current therapeutic options. The rate of relapse is fairly consistent over time, even in patients who have achieved complete responses to treatment.[8] Watchful waiting, the deferring of treatment until the patient becomes symptomatic, is an option for patients with advanced-stage follicular lymphoma.[9,10] An international index for follicular lymphoma (the Follicular Lymphoma International Prognostic Index [FLIPI]) [11,12,13] identified five significant risk factors prognostic of overall survival (OS):
- Age (≤60 years vs. >60 years).
- Serum lactate dehydrogenase (LDH) (normal vs. elevated).
- Stage (stage I or stage II vs. stage III or stage IV).
- Hemoglobin level (≥120 g/L vs. <120 g/L).
- Number of nodal areas (≤4 vs. >4).
Patients with fewer than two risk factors have a 10-year survival rate of 85%, and three or more risk factors confer a 10-year survival rate of 40%.[11] In a revised FLIPI-2, an elevated beta-2-microglobulin and lymph node size of more than 6 cm are proposed prognostic factors instead of serum LDH and the number of nodal areas.[14] Although the FLIPI and FLIPI-2 indices can predict progression-free survival (PFS) and OS, the scores cannot be used to establish the need for therapy or to predict response to therapy.[11,14] The primary use of FLIPI or FLIPI-2 is to assure a balance of prognostic factors or to define entry requirements in randomized clinical trials. Individuals with an adverse FLIPI score may well benefit from watchful waiting or may respond well to initial therapy. An alternative prognostic index using only beta-2-microglobulin and initial bone marrow involvement (PRIMA-PI) has the disadvantage of requiring an invasive test not usually required outside the context of a clinical trial.[15] An alternative prognostic index using only noninvasive clinical variables outperformed FLIPI, FLIPI-2, and PRIMA-PI, using data from immunochemotherapy trials.[16]
Three retrospective analyses, including one pooled analysis of 5,225 patients from 13 randomized clinical trials, identified a high-risk group that had a 5-year OS rate of 50% when relapses occurred within 24 months of induction chemoimmunotherapy.[17,18,19] A fourth retrospective analysis of 296 patients who received bendamustine and rituximab found a 2-year OS rate of 38% (95% confidence interval [CI], 20%−55%) among those with progression of disease before 24 months (POD24). Most of these patients (76%) had transformed disease (histological progression to diffuse large B-cell lymphoma [DLBCL]).[20] These patients with higher-risk POD24 disease represent a target population for clinical trials.
Therapeutic approaches
Because of the often-indolent clinical course and the lack of symptoms in some patients with follicular lymphoma, watchful waiting remains a standard of care during the initial encounter and for patients with slow asymptomatic relapsing disease. When therapy is required, numerous options may be used in varying sequences with an OS equivalence at 5 to 10 years.[9,21,22,23] Rituximab can be given alone or in combination with various chemotherapy options.[23,24,25] Rituximab can also be combined with the immunomodulating-agent lenalidomide to avoid the short- and long-term toxicities of cytotoxic agents.[26,27,28] Obinutuzumab is a completely humanized anti–CD20 monoclonal antibody that can be given alone or with combination chemotherapy. It may be especially useful for patients who develop severe allergic reactions to rituximab due to human antimouse antibodies.[29] CD19-directed chimeric antigen receptor T cells may be used in patients who have disease progression after two or more prior lines of therapy.[30] Mosunetuzumab, a bispecific CD20-directed CD3 T-cell engager, may also be used in this setting.[31] Consolidation therapy for relapsed disease after reinduction therapy using autologous stem cell transplant (SCT) or allogeneic SCT can be considered.[32]
Outside the context of clinical trials, the use of measurable residual disease (MRD) testing has not been shown to be predictive in directing therapy for patients with follicular lymphoma. In retrospective analyses of two randomized prospective trials, while MRD negativity was prognostic of outcome, maintenance rituximab or obinutuzumab prolonged PFS the most among patients with MRD-negative disease.[33,34][Level of evidence C2] Stopping maintenance rituximab or obinutuzumab was not indicated in patients with MRD-negative disease, negating any possible change in therapy based on that status.
Follicular lymphoma in situ and primary follicular lymphoma of the duodenum are particularly indolent variants that rarely progress or require therapy.[35,36] A so-called pediatric-type nodal follicular lymphoma has indolent behavior and rarely recurs; adult patients with this histological variant have disease characterized by a lack of BCL2 rearrangement in conjunction with a Ki-67 proliferation index greater than 30% and a localized stage I presentation.[37]
Patients with indolent lymphoma may experience a relapse with a more aggressive histology. If the clinical pattern of relapse suggests that the disease is behaving in a more aggressive manner, a biopsy can be performed, if feasible.[38] If disease conversion to a more aggressive histology is confirmed, therapy must change to a regimen applicable to that histological type.[39] Rapid growth or discordant growth between various disease sites may indicate a histological conversion.[38] In a retrospective review of 325 patients diagnosed between 1972 and 1999, the 10-year risk of histological transformation was 30%.[40] In this series, high-risk factors for subsequent histological transformation were advanced stage, high-risk FLIPI, and watchful waiting (as opposed to treatment being initiated at diagnosis). The 5-year OS rate was more than 50% for patients who had biopsy-proven, aggressive-histology transformation in several multicenter cohort studies using rituximab plus anthracycline or platinum-based chemotherapy, or similar therapy followed by autologous or allogeneic SCT.[38,41,42]
In a prospective nonrandomized study, at a median follow-up of 6.8 years, 379 of 2,652 patients (14%) subsequently transformed to a more aggressive histology after an initial diagnosis of follicular lymphoma.[43][Level of evidence C3] The median OS after subsequent transformation was 5 years. However, among 47 patients with evidence of transformation in conjunction with follicular lymphoma at the time of initial diagnosis, the OS was no worse than that of the nontransformed patients (5-year OS rate, 88%; 95% CI, 74%–95%).
Grade 3b follicular lymphoma is managed similarly to DLBCL. For more information, see Aggressive B-Cell Non-Hodgkin Lymphoma Treatment.
Lymphoplasmacytic Lymphoma (Waldenström Macroglobulinemia)
Lymphoplasmacytic lymphoma is usually associated with a monoclonal serum paraprotein of immunoglobulin M (IgM) type (Waldenström macroglobulinemia).[44] Most patients have bone marrow, lymph node, and splenic involvement, and some patients may develop hyperviscosity syndrome. Most patients with Waldenström macroglobulinemia carry the MYD88 variant, which some pathologists consider indicative for the disease.[45] Other lymphomas may also be associated with serum paraproteins. Patients with lymphoplasmacytic lymphoma should be checked for associated hepatitis C virus (HCV) infection.
Asymptomatic patients can be monitored for evidence of disease progression without immediate need for chemotherapy.[9,46,47]
Prognostic factors associated with symptoms requiring therapy include:
- Aged 70 years or older.
- Beta-2-microglobulin of 3 mg/dL or more.
- Increased serum LDH.[46]
An externally validated prognostic model uses age, albumin, and LDH levels.[48]
Therapeutic approaches
The management of lymphoplasmacytic lymphoma is similar to that of other low-grade lymphomas, especially diffuse small lymphocytic lymphoma/chronic lymphocytic leukemia.[49,50,51] If the serum viscosity relative to water is greater than four, the patient may have symptoms of hyperviscosity. Plasmapheresis is useful for temporary, acute symptoms such as retinopathy, congestive heart failure, and central nervous system (CNS) dysfunction. It can also be combined with chemotherapy for prolonged disease control. Symptomatic patients with a serum viscosity of four or lower are usually treated with chemoimmunotherapy or biologically directed therapies. Therapy may be required to correct hemolytic anemia in patients with chronic cold agglutinin disease; rituximab, bendamustine, and steroids are often used.[47] Occasionally, a heated room is required for patients whose cold agglutinins become activated by even minor chilling. Sutimlimab, an immunoglobulin G4 monoclonal antibody that selectively inhibits the complement pathway at C15, can reduce hemolysis when therapies directed at the lymphoplasmacytic lymphoma are ineffective.[52]
First-line regimens include zanubrutinib (a Bruton tyrosine kinase [BTK] inhibitor), rituximab, and ibrutinib (another BTK inhibitor), rituximab alone, the nucleoside analogues, and alkylating agents, either as single agents or as part of combination chemotherapy.[53,54,55,56] In a randomized prospective trial, 150 symptomatic patients (including patients with previously untreated and relapsing disease) received either ibrutinib and rituximab or rituximab and a placebo. With a median follow-up of 50 months, the 4.5-year PFS rate was 68% in the ibrutinib-and-rituximab arm (95% CI, 55%–78%) and 25% in the rituximab-and-placebo arm (95% CI, 15%–37%) (hazard ratio [HR], 0.25; 95% CI, 0.15–0.42; P < .0001). The OS rate at 30 months was no different in the two arms (92%–94%).[55][Level of evidence B1] Zanubrutinib was compared with ibrutinib in a randomized prospective clinical trial of 164 patients with relapsed disease and 38 with previously untreated disease.[56] With a median follow-up of 44.4 months, the PFS rate was similar in both groups at 70% to 78% (HR, 0.63; 95% CI, 0.36–1.12), and the OS rate was similar in both groups at 85% to 87% (HR, 0.75; 95% CI, 0.36–1.59).[57] The zanubrutinib group had fewer cases of atrial fibrillation (11 vs. 1) and 50% fewer cases of hypertension (statistics not provided).[56][Level of evidence C3] BTK inhibition with ibrutinib allowed all 13 patients with cold-antibody–mediated autoimmune hemolytic anemia and acrocyanosis to attain clinical remission regardless of underlying pathology or MYD88 variant status.[58][Level of evidence C3]
Previously untreated patients who received rituximab had response rates of 60% to 80%, but close monitoring of the serum IgM is required because of a sudden rise in this paraprotein at the start of therapy.[59,60,61][Level of evidence C3] The rise of IgM after rituximab can be avoided with the concomitant use of an alkylating agent, such as cyclophosphamide, or the proteosome inhibitors bortezomib or ixazomib.[47,62,63,64] A combination of bortezomib, dexamethasone, and rituximab has been used without causing IgM rebound.[65,66,67] Previously untreated patients with lymphoplasmacytic lymphoma who received the nucleoside analogues cladribine and fludarabine showed similar response rates.[54,68,69][Level of evidence C3] Patients who received single-agent alkylators, bendamustine, bortezomib, venetoclax, and combination chemotherapy with or without rituximab also showed similar response rates.[54,62,64,70,71,72,73,74][Level of evidence C3] In the rare case of lymphoplasmacytic lymphoma involving the CNS (Bing-Neel syndrome), ibrutinib resulted in an 85% response rate in an anecdotal series of 28 patients.[75][Level of evidence C3]
Myeloablative therapy with autologous or allogeneic hematopoietic stem cell support is under clinical evaluation.[76,77,78,79] Candidates for this approach should avoid long-term use of alkylating agents or purine nucleoside analogues, which can deplete hematopoietic stem cells or predispose patients to myelodysplasia or acute leukemia.[59,80] After relapse from alkylating-agent therapy, 92 patients with lymphoplasmacytic lymphoma were randomly assigned to receive either fludarabine or cyclophosphamide, doxorubicin, and prednisone. Although relapse-free survival favored fludarabine (median duration of 19 months vs. 3 months; P < .01), no difference was observed in OS.[81][Level of evidence B1]
Marginal Zone Lymphoma
When marginal zone lymphomas involve the nodes, they are called monocytoid B-cell lymphomas or nodal marginal zone B-cell lymphomas. When they involve extranodal sites (e.g., gastrointestinal tract, thyroid, lung, breast, orbit, and skin), they are called mucosa-associated lymphatic tissue (MALT) lymphomas.[82,83] Splenic marginal zone lymphoma is a distinct clinical entity, which usually presents with massive splenomegaly. A variant form of MALT lymphoma is known as immunoproliferative small intestinal disease (IPSID).[83] A prognostic index for all of the marginal zone lymphomas has three adverse prognostic factors: aged 70 years or older, stage III or stage IV disease, and high LDH level.[84] Fewer than 10% of patients transform to a higher-grade lymphoma. In one retrospective review, risk factors for transformation included elevated LDH, more than four nodal sites at the time of initial diagnosis of marginal zone lymphoma, and failure to achieve complete response after initial treatment.[85]
Gastric MALT
Many patients have a history of autoimmune disease, such as Hashimoto thyroiditis or Sjögren syndrome, or of Helicobacter gastritis. Most patients present with stage I or stage II extranodal disease, which is most often in the stomach. Treatment of H. pylori infection may resolve most cases of localized gastric involvement.[86,87] After standard antibiotic regimens, 50% of patients show resolution of gastric MALT by endoscopy after 3 months. Other patients may show resolution after 12 to 18 months of observation. Of the patients who attain complete remission, 30% demonstrate monoclonality by immunoglobulin heavy chain rearrangement on stomach biopsies with a 5-year median follow-up.[88] The clinical implication of this finding is unknown. Translocation t(11;18) in patients with gastric MALT predicts poor response to both antibiotic therapy and oral alkylator therapy, and predicts negative H. pylori testing results.[89,90,91] Patients with stable asymptomatic disease and persistently positive biopsies have been successfully followed with a watchful waiting approach until disease progression.[87] Patients with disease progression are treated with radiation therapy,[92,93,94,95,96,97] rituximab,[98] surgery (total gastrectomy or partial gastrectomy plus radiation therapy),[99] chemotherapy,[100] or combined-modality therapy.[101] A single-arm prospective trial enrolled 24 patients with newly diagnosed or relapsed H. pylori –negative gastric MALT.[97] Most patients had a complete response to radiation therapy at 4 Gy, and 20 Gy was applied as salvage therapy. The 3-year local control rate was 96% (95% CI, 88%–100%).[97][Level of evidence C3] Endoscopic ultrasonography may help clinicians monitor responses in these patients.[102] Four case series encompassing more than 100 patients with stage IE or IIE DLBCL with or without associated MALT (but H. pylori -positive) reported durable complete remissions in more than 50% of the patients after treatment of H. pylori.[103,104,105,106]
Extragastric MALT
Localized involvement of other sites can be treated with radiation therapy or surgery.[93,94,95,107,108,109,110] Patients with extragastric MALT lymphoma have a higher relapse rate than patients with gastric MALT lymphoma in some series, and relapses can happen many years and even decades later.[111] Many of these recurrences involve different MALT sites than the original location.[112] When disseminated to lymph nodes, bone marrow, or blood, this entity behaves like other low-grade lymphomas.[113,114] A prospective randomized trial of 401 patients with nongastric extranodal MALT compared chlorambucil alone versus rituximab plus chlorambucil versus rituximab alone.[115] With a median follow-up of 7.4 years, the event-free survival was 68% in the rituximab-plus-chlorambucil arm, 51% in the rituximab-alone arm, and 50% in the chlorambucil-alone arm (P = .0009). However, the 5-year OS rate was 90% in all arms.[115] For patients with ocular adnexal MALT, antibiotic therapy using doxycycline that targeted Chlamydia psittaci resulted in durable remissions for almost one-half of the patients in a review of the literature that included 131 patients.[116][Level of evidence C3] These responses to doxycycline are mainly seen in Italian trials and less often in trials conducted in other geographic sites.[117] Large B-cell lymphomas of MALT sites are classified and treated as diffuse large cell lymphomas.[118] A large, retrospective review of primary ocular adnexal MALT found that after 10 years of follow-up, 4% of stage I patients treated with radiation therapy had disease transformation to DLBCL, and 3% developed CNS involvement.[119]
Nodal marginal zone lymphoma
Patients with nodal marginal zone lymphoma (monocytoid B-cell lymphoma) are treated with watchful waiting or therapies as described for lymphoplasmacytic lymphoma. Rituximab alone, obinutuzumab alone, or combinations with cytotoxic agents (such as bendamustine, CVP [cyclophosphamide, vincristine, and prednisone] or CHOP [cyclophosphamide, doxorubicin, vincristine, and prednisone]) can be used.[120,121,122][Level of evidence C3] Zanubrutinib is approved for patients with disease relapse after a rituximab-containing regimen. This approval was based on a single-arm phase II study.[123] With a median follow-up of 15.7 months, the overall response rate was 68.2%, and the complete response rate was 25.8%. The median duration of response was 93% at 12 months.[123][Level of evidence C3] Ibrutinib also showed similar efficacy in patients with relapsed marginal zone lymphoma.[124][Level of evidence C3] Patients with marginal zone lymphoma comprised a small percentage (about 15%) of the population for a trial that established the benefit of rituximab with lenalidomide in patients with relapsed or refractory indolent lymphoma (AUGMENT trial).[125][Level of evidence C3] Similar to follicular lymphoma, patients with POD24 who required initiation of therapy had a worse prognosis than did the patients without POD24 (3-year OS rate, 53% vs. 95%).[126] Among patients with concomitant HCV infection, 40% to 60% attained a complete or partial remission after loss of detectable HCV RNA with antiviral treatment.[127,128][Level of evidence C3]
Mediterranean abdominal lymphoma
The disease variously known as Mediterranean abdominal lymphoma, heavy-chain disease, or IPSID, which occurs in young adults in eastern Mediterranean countries, is another version of MALT lymphoma. This disease responds to antibiotics in its early stages.[129]Campylobacter jejuni has been identified as one of the bacterial species associated with IPSID, and antibiotic therapy may result in disease remission.[130]
Splenic marginal zone lymphoma
Splenic marginal zone lymphoma is an indolent lymphoma that is marked by massive splenomegaly and peripheral blood and bone marrow involvement, usually without adenopathy.[131,132] This type of lymphoma is also known as splenic lymphoma with villous lymphocytes. Splenectomy may result in prolonged remission.[133,134]
Management is similar to that of other low-grade lymphomas and usually involves rituximab alone or rituximab in combination with purine analogues or alkylating agent chemotherapy.[135] Splenic marginal zone lymphoma responds less well to chemotherapy, which would ordinarily be effective for chronic lymphocytic leukemia.[131,135,136] Among small numbers of patients with splenic marginal zone lymphoma (splenic lymphoma with villous lymphocytes) and HCV infection, most attained a complete or partial remission after loss of detectable HCV RNA with treatment using interferon-alpha with or without ribavirin.[127,137]; [138][Level of evidence C3] In contrast, no responses to interferon were seen in six HCV-negative patients.
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