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© 2003 American Society for Clinical Oncology Localized Mucosa-Associated Lymphoid Tissue Lymphoma Treated With Radiation Therapy Has Excellent Clinical Outcome
From the Departments of Radiation Oncology and Biostatistics, Medical Oncology-Hematology, and Pathology, Princess Margaret Hospital, University Health Network, University of Toronto, Toronto, Canada. Address reprint requests to Richard Tsang, MD, Department of Radiation Oncology, Princess Margaret Hospital, 610 University Ave, Toronto, Ontario M5G 2M9, Canada; e-mail: richard.tsang{at}rmp.uhn.on.ca.
Purpose: Extranodal marginal zone B-cell lymphoma of mucosa-associated lymphoid tissue (MALT lymphoma) is a distinct lymphoma with unique clinicopathologic features. We report the clinical outcome of stage I and II MALT lymphoma treated with involved field radiation therapy (RT). Patients and Methods: From 1989 to 2000, 103 patients with stage IE and IIE disease were referred. Their median age was 60 years, with a 2:1 female predominance. Presenting sites were stomach (17 patients), orbital adnexa (31 patients), salivary glands (24 patients), thyroid gland (13 patients), and other sites (18 patients). Ninety-three patients received RT—85 received RT alone, and eight received chemotherapy and RT—with a median dose of 30 Gy. The median follow-up time was 5.1 years. Results: A complete response (CR) to RT alone was achieved in 84 of 85 patients. Among CR patients, 14 experienced relapse. Relapse sites were mostly contralateral paired-organ or distant MALT locations and, infrequently, lymph nodes. The crude local control rate with RT was 95.3% (81 of 85 patients). No relapses were observed in patients with stomach or thyroid lymphoma, whereas 14 of 63 patients (22%) experienced relapse in the other sites. The overall 5-year survival rate was 98%, and the disease-free survival rate was 77%. Transformed lymphoma was observed in 14% of patients (two of 14) experiencing relapse. Conclusion: Moderate-dose RT achieved excellent local control in localized MALT lymphomas and had curative potential for three fourths of the patients. Gastric and thyroid MALT lymphomas had better outcome, whereas distant failures were common for other sites. Despite relapse, the disease often maintained an indolent course.
MUCOSA-ASSOCIATED LYMPHOID tissue (MALT) lymphoma was first described by Isaacson and Wright in 19831 and is now recognized as a distinct lymphoma with unique clinicopathologic features.2–4 However, the etiology, sites of presentation, and biologic behavior remain variable and heterogeneous. MALT lymphoma accounts for 4% to 13% of patients seen in individual cancer centers,5,6 and approximately 70% of patients with MALT lymphoma present with stage I or stage II disease.6–8 In gastric MALT lymphoma associated with Helicobacter pylori, therapy to eradicate this microorganism results in a 55% to 80% complete regression of MALT lymphoma.9–14 Patients who are resistant to H pylori eradication therapy require more traditional cytotoxic treatments, such as chemotherapy and radiation therapy (RT). Tumors with the chromosomal translocation t(11;18)(q21;q21) in gastric MALT lymphoma are usually resistant to antibiotic therapy.15,16 For MALT lymphomas arising in nongastric locations, etiologic agents have not been identified,17,18 except anecdotally; for example, Borrelia burgdorferi in cutaneous lymphoma19 and Chlamydia psittaci in ocular adnexal lymphoma.20 However, predisposing conditions to MALT lymphoma of some specific sites are well recognized: for example, Hashimoto’s thyroiditis for thyroid MALT lymphoma21 and Sjögren’s syndrome for salivary gland MALT lymphoma.22,23 Treatment approaches for MALT lymphomas are still evolving. Because MALT lymphomas tend to remain localized for a long time, local treatments, such as RT, are an attractive treatment strategy. To date, there are few well-documented reports of the efficacy of RT in this disease. We report our experience of involved-field RT for stage I and II MALT lymphomas, documenting the excellent local control with RT and the indolent nature of the disease despite relapse.
Patients We reviewed the records of 103 consecutive patients with biopsy-proven diagnosis of stage I or II MALT lymphoma presenting in extralymphatic organs between 1989 and 2000 and treated at Princess Margaret Hospital (PMH; Toronto, Ontario, Canada). All histologic material was reviewed by the PMH hematopathologists, with appropriate immunophenotypic techniques establishing the diagnosis. Patients with transformed lymphoma (MALT lymphoma with areas of diffuse large-cell lymphoma) were not included in this study. Staging included CBC in 99 patients (96%), lactate dehydrogenase (LDH) level in 71 patients (69%), appropriate site-specific imaging, and chest x-ray or computed tomography (CT) of the thorax in 68 patients (66%). CT of the abdomen and pelvis was performed in 95 patients (92%), gallium scan in 44 patients (43%), and bone marrow biopsy in 82 patients (80%). Upper endoscopy and gastric biopsies were performed in all patients with gastric lymphoma, but not in the patients with nongastric disease. H pylori was documented in biopsy specimens in eight of 15 patients with gastric lymphoma.
Treatment
Response assessment was performed at 2 to 6 months after RT with clinical examination and imaging of the affected area (computed tomography or MRI as appropriate). Routine endoscopy was performed for gastric lymphoma patients every 4 to 6 months for 2 to 3 years. Patients were seen in clinic with physical examination and routine CBC and LDH level (every 3 to 4 months for 2 years, then every 6 months up to the fifth year, then yearly), with no additional routine imaging test. The median follow-up time for all patients was 5.3 years (range, 1 to 13.4 years), and 4.9 years (range, 1 to 10.7 years) for the RT-alone group.
Statistical Analysis
Patients Patient characteristics, including the presenting sites, are listed in Table 3  . Among the 24 salivary gland lymphomas, 20 were located in the parotid gland. Among the 31 orbital lymphomas, there were 12 conjunctival lesions, nine lacrimal gland lesions, eight periorbital soft tissue lesions, and two eyelid lesions. For the 12 patients with stage IIE disease (regional lymph node involved), the sites were thyroid (one patient, cervical node), salivary gland (five patients, upper cervical nodes), lung (one patient, hilar; one patient, mediastinal nodes), and stomach (two patients, paragastric nodes; two patients, celiac nodes).
Treatment Outcome—Surgery Only and H pylori Eradication Only Among the five patients treated with surgical excision only, two experienced relapse locally (lung and minor salivary gland in oral cavity). Both patients were subsequently treated with chemotherapy (oral chlorambucil), had partial responses, and are alive with disease at last follow-up (12 and 9 years from initial diagnosis, respectively). Three patients had complete surgical excision for stage IE MALT lymphoma in the lung, submandibular salivary gland, and stomach, and were free of recurrent disease after 5.5, 8.5, and 7.1 years of follow-up, respectively. Two patients with gastric MALT lymphoma treated with H pylori eradication therapy only were free of recurrent disease after 4.5 and 6 years of follow-up, respectively.
Treatment Outcome—Chemotherapy With RT
Treatment Outcome—RT Alone
Side Effects of RT RT was well tolerated, with no serious acute toxicity observed. Patients with orbital lymphoma often developed a cataract, 2 to 5 years after treatment, which was successfully treated with surgical extraction. When appropriate lens shielding was possible, the risk of cataracts was reduced to 10%. Patients with gastric lymphoma developed transient anorexia and malaise and occasional nausea or dyspepsia, and were treated conservatively. Late ulceration or hemorrhage was not observed. Patients with Sjögren’s syndrome and MALT lymphoma of salivary glands had significant residual xerostomia after RT, which was often symptomatic and required permanent modifications in their dietary habits (eg, sipping fluid frequently during meals). Patients with lung lymphoma manifested imaging evidence of radiation pneumonitis after treatment, evolving in the irradiated lung tissue into permanent but nonprogressive fibrosis, and were clinically asymptomatic. Nine patients had second cancers (Table 5 ). One of these patients died from metastatic adenocarcinoma of the pancreas, with the second cancer located within the previous radiation field given for MALT lymphoma of the stomach, whereas seven second cancers occurred outside the RT field.
Treatment Outcome After Relapse—RT With or Without Chemotherapy Among 16 patients experiencing treatment failure for whom the initial treatment was RT with or without chemotherapy, there were two patients for whom treatment failed in the local site only (both orbital MALT lymphoma; one such patient died as a result of salvage treatment and lymphoma 5 years after initial diagnosis). The other patient was diagnosed with in-field relapse in the conjunctiva 3.5 years after RT (25 Gy) and was not assessable because of short follow-up. Among the five patients with contralateral organ relapse (orbital, three patients; parotid, two patients), all received RT, achieved CR, and remain disease-free 0.7 to 5.4 years from relapse (average follow-up, 3.0 years from relapse). Two patients with parotid lymphoma experienced treatment failure both locally and at distant sites. One patient’s disease relapsed 3 years after an incomplete course of local RT—the patient refused treatment after receiving 17.5 Gy—with parotid, neck node, and bone marrow involvement. She was treated with chemotherapy and remains alive with disease 2.6 years after relapse. The other patient (with parotid MALT lymphoma) experienced relapse 1 year after RT (30 Gy), locally and at distant sites, including the kidneys, and received chemotherapy with partial response. He is alive with disease 1.9 years after relapse. Among the seven patients who experienced relapse exclusively at distant sites, six were re-treated with RT and/or chemotherapy, and five achieved CR and remain alive and free of disease 1.9 to 6.2 years from relapse (average follow-up, 4.0 years from relapse). This included the two patients with transformed lymphoma. One patient with orbital lymphoma experienced disease recurrence with a solitary lung nodule, biopsy-proven to be MALT lymphoma, and has been observed without treatment for 2 years with no progression of disease. Therefore, among the 16 patients with residual or recurrent MALT lymphoma, 10 (63%) were rendered disease free again with additional courses of RT (seven patients), chemotherapy (one patient), and CMT (two patients), with a median follow-up of 3.8 years from first relapse.
Prognostic Factors for Treatment Failure
MALT lymphoma, a term used synonymously with extranodal marginal zone B-cell lymphoma (MZL), is a distinct type of B-cell lymphoma.2–4 Characteristic genetic abnormalities can include trisomy 326 and chromosomal translocations t(11;18)(q21;q21),27–32 t(1;14)(p22;q32),33 and t(14;18)(q32;q21).34 The t(11;18) translocation resulting in an API2-MLT fusion transcript, although implicated in the molecular pathogenesis of gastric MALT lymphomas,29,35 has also been reported to associate with resistance to H pylori eradication therapy.16 That t(11;18) translocation is also found in MALT lymphoma arising from nongastric sites such as lung and orbit27 suggests a common genetic mechanism in the development of disease in these sites for some patients, but not in those with other sites (salivary gland, thyroid gland) where abnormal autoimmune response may be implicated. The median age (60 years) and female predominance in our series are similar to other reports in the literature.7,8,36–38 The distribution of anatomic sites in our patients differs from that in other series, with the four most common sites in our patients being orbit, stomach, salivary gland, and thyroid. This distribution of anatomic sites probably reflects local referral patterns because of the specialized surgical and radiation oncology programs and expertise (eg, orbital tumor program) of our institution, as well as the local prevalence of the predisposing conditions (eg, H pylori infection in stomach lymphomas). Other series have a higher proportion of stomach,7 lung,38 salivary,8 or skin lymphomas.7,8,38 Our data showed that MALT lymphomas respond extremely well to moderate-dose RT, with a high CR rate and durable local control. This study updated and expanded on our previous report of 70 patients,39 with longer follow-up and an emphasis on the outcome of patients with relapsed disease after initial management. Similar to our experience, Schechter et al40 reported a local control rate of 100% in 17 patients with stage I and II gastric MALT lymphomas. Liao et al36 also reported durable local disease control in all 14 stage I and II patients with nongastric MALT lymphoma who were managed with RT with or without chemotherapy. However, local failure is still infrequently observed, particularly if the RT dose is less than 30 Gy; this could be a contributory factor in two of our patients who experienced local relapse after 17.5 and 25 Gy, respectively. More importantly, we observed a pattern of preferential recurrence in paired organs and in distant mucosal sites. This has also been documented by other investigators, who reported spleen41 and diverse mucosal site involvement that may include the bone marrow either at diagnosis or at relapse.7,8,37,38,42 The majority of our patients experienced relapse in a localized fashion, either in the contralateral paired organ or other mucosa-associated sites, and were treated with a second course of RT (with or without chemotherapy) and achieved control of disease once again. The median duration of follow-up from first relapse is less than 4 years, and additional observation will determine if these second remissions are durable. Our overall 5-year DFS of 77% is comparable with those reported in the literature.7,8,36,38 Despite recurrence of MALT lymphoma, the disease behaves in an indolent fashion, and we have observed continued survival of all patients who experienced relapse. Regardless of whether the initial treatment cures the disease, prolonged survival is highly likely given that it has also been reported by other investigators. The 5-year survival was 95% in 75 patients with nongastric MALT lymphomas from Italy,38 and a 10-year survival estimate of 80% was documented among 158 patients with stage I to IV disease from France.7 Patients with stage III and IV disease also have an indolent course.7,8,36 However, the experience reported by the Southwest Oncology Group43 showed a 10-year survival of only 39% in a retrospective analysis of 43 patients who received cyclophosphamide, doxorubicin, vincristine, and prednisone chemotherapy in their clinical trials. These patients were reclassified as having MZL by subsequent pathologic review; 44% of them (19 of 43 patients) had disease involving a MALT site, with or without nodal disease.43 The nodal and splenic subtypes of MZL usually present in advanced stages (III and IV). They tend to behave in an indolent fashion as well, with one recent series of 124 patients having a median survival time of 9.1 years.44 However, the nodal subtype of MZL has also been reported to have a poorer prognosis in comparison with MALT lymphomas, even when corrected for the International Prognostic Index score.45 The fact that these are separate disease entities from MALT lymphoma is also supported by the lack of the t(11;18)(q21;q21) translocation in nodal MZL.29,32
Our data showed no relapses in gastric and thyroid MALT lymphomas treated with RT with or without chemotherapy (Fig 2 Patients who present with thyroid involvement also have an excellent outcome. The series of nongastric MALT lymphomas reported by Zinzani et al38 showed no relapses in the seven patients with thyroid MALT lymphomas, in contrast to other sites (lung, orbit, and skin), for which the relapse rate was 20% to 30%. Similarly, Zucca et al8 reported no relapses in the 10 patients with thyroid lymphoma but much higher relapse rates for the other sites. Patients treated with thyroidectomy in one small series had excellent outcome.47 Therefore, the role of RT is unclear if a patient undergoes complete tumor excision with total thyroidectomy. There is extensive documentation of excellent local control with RT in orbital lymphomas48,49 and small series of patients for the other sites.50–53 Patients generally tolerate treatment well, and long-term toxicity is infrequent. However, the risk of relapse in distant extranodal sites remains a significant problem.8,54 Therefore, it is tantalizing to consider an initial role for chemotherapy in this disease,54 although this has not been extensively studied. One multi-institutional study of 180 patients with stage I to IV disease did not find a difference in clinical outcome between initial localized treatment approaches with systemic chemotherapy.8 Consequently, chemotherapy does not seem necessary for patients with MALT lymphomas, at least in the early stages, when the disease remains localized. Oral alkylating drugs, such as chlorambucil, cyclophosphamide, and 2-chlorodeoxyadenosine, appear to be active agents14,55,56 and can be considered for more advanced stages of the disease. Given that the majority of MALT lymphoma cells express CD20, rituximab has been reported to have significant clinical activity, with a response rate of 73% in 34 patients so treated, and a median response duration of 10.5 months.57 We observed nine subsequent cancers in this series, but only one arose within the radiation field (adenocarcinoma of pancreas, with liver metastasis) 5 years after RT to the stomach. Some series reported a higher incidence of other malignancies in patients with MALT lymphomas,58,59 but not in another series.60 In light of the high local control rate and low incidence of toxicity, together with the indolent biology of the disease, we conclude that moderate-dose RT (25 to 30 Gy) is a safe and effective choice for stage I and II MALT lymphomas.
The authors indicated no potential conflicts of interest.
Presented in part at the 44th Annual Meeting of the American Society for Therapeutic Radiology and Oncology, New Orleans, LA, October 2002.
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ABSTRACT
INTRODUCTION
