This Article Abstract Full Text (PDF) Purchase Article View Shopping Cart Alert me when this article is cited Alert me if a correction is posted Services Email this article to a colleague Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Save to my personal folders Download to citation manager Rights & Permissions Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Zinzani, P. L. Articles by Tura, S. Search for Related Content PubMed PubMed Citation Articles by Zinzani, P. L. Articles by Tura, S.

Nongastrointestinal Low-Grade Mucosa-Associated Lymphoid Tissue Lymphoma: Analysis of 75 Patients

From the Institute of Hematology and Medical Oncology "Seràgnoli," University of Bologna, Bologna; Hematology Division, University of Siena, Siena; Chair of Hematology "La Sapienza," Rome; Division of Pulmonary Medicine, Maggiore Hospital, Bologna; Chair of Hematology, University of Udine, Udine; Hematology Division, Catanzaro Hospital, Catanzaro; Hematology Division, Ravenna Hospital, Ravenna; Chair of Hematology "Tor Vergata," Rome; Oncology Division, Forlì Hospital, Forlì; and Hematology Unit, Cesena Hospital, Cesena, Italy.

Address reprint requests to Pier Luigi Zinzani, MD, Istituto di Ematologia e Oncologia Medica, Policlinico S. Orsola, Via Massarenti 9, 40138 Bologna, Italy; email seragnol{at}kaiser.alma.unibo.it

	ABSTRACT

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION REFERENCES

 
PURPOSE: Nongastrointestinal locations represent about 30% to 40% of all low-grade mucosa-associated lymphoid tissue (MALT) lymphomas. We report a retrospective analysis of 75 patients with nongastrointestinal low-grade MALT lymphoma, presenting their clinical, therapeutic, and follow-up data with respect to the initial location of the lymphoma.

PATIENTS AND METHODS: From January 1988 to October 1997, 75 patients with untreated nongastrointestinal low-grade MALT lymphoma were subjected to treatments ranging from local radiotherapy and local interferon alfa administration to chemotherapy. The lymphomas were located in the lung (19 patients), orbital soft tissue (16 patients), skin (seven patients), thyroid (seven patients), lachrymal gland (six patients), conjunctiva (six patients), salivary gland (six patients), breast (three patients), eyelid (two patients), larynx (one patient), bone marrow (one patient), and trachea (one patient).

RESULTS: Complete and partial remissions were achieved in 59 (79%) and 16 (21%) of the 75 patients, respectively, with an overall response rate of 100%. All but two of the patients are still alive, with a median follow-up of 47 months; these two patients died from other causes. The estimated time to treatment failure rate is 30% at 5 years. In the thyroid and lachrymal gland sites, no relapses were reported.

CONCLUSION: Our data regarding the largest reported series of nongastrointestinal MALT lymphomas confirm the good prognosis of this particular clinicopathologic entity and the significant efficacy of different therapeutic approaches to specific sites.

	INTRODUCTION

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION REFERENCES

 
MUCOSA-ASSOCIATED LYMPHOID tissue (MALT) lymphomas were first described by Isaacson and Wright¹ in 1983 in a small series of patients with low-grade B-cell gastrointestinal lymphomas. Although MALT lymphomas occur most frequently in the stomach, they have also been described in various nongastrointestinal sites, such as salivary gland, conjunctiva, thyroid, orbit, lung, breast, kidney, skin, liver, and prostate.^2-18 This particular entity was not included in the Working Formulation for Clinical Usage¹⁹; however, in the updated Kiel classification,²⁰ it was listed as a monocytoid cell lymphoma; in the revised European-American lymphoma (R.E.A.L.) classification²¹ of 1994, the MALT lymphomas were definitively classified among the marginal zone B-cell lymphomas.

MALT lymphomas are characterized by neoplastic marginal cells, which display a variable combination of colonization of reactive germinal centers, plasmacytic differentiation, and destructive epithelial infiltration, forming lymphoepithelial lesions. The risk of a diagnostic dilemma is reduced by the favorable prognosis of this low-grade lymphoma and its tendency to remain localized to the primary site for a long time. Paradoxically, MALT lymphomas only occasionally arise from sites where MALT is normally present, such as the tonsil and Peyer's patches. The reason for this seems to be that MALT lymphomas generally arise in lymphoid tissue that has been acquired as a result of some pre-existing disorder, eg, Helicobacter pylori colonization in the stomach,^22,23 follicular bronchiectasis in the lung,²⁴ autoimmune diseases in the salivary gland (Sjögren's disease) and thyroid gland (Hashimoto's thyroiditis),^25,26 and reactive or inflammatory lesions of the orbit lymphoma.²⁷ The literature contains reports of a correlation between hepatitis C virus infection and extranodal MALT lymphomas.^28-30 With regard to therapy, in contrast to nodal lymphomas, low-grade MALT lymphomas respond favorably to local treatments such as surgery and/or local radiation therapy. The outcome and prognosis for low-grade MALT lymphomas are more favorable than for other extranodal lymphomas. In this article, we report retrospectively on 75 consecutive patients with untreated nongastrointestinal MALT lymphoma, focusing on their clinical features at presentation, therapeutic approaches, and follow-up data.

	PATIENTS AND METHODS

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION REFERENCES

 
From January 1988 to October 1997, 75 patients with previously untreated nongastrointestinal MALT lymphoma were admitted to nine Italian institutions. Until 1994, the histologic and cytologic diagnosis of MALT lymphoma was made according to the updated Kiel classification,²⁰ thereafter, the R.E.A.L. classification²¹ was used. For the purposes of this study, the exact diagnoses of all patients were reviewed according to the R.E.A.L. classification. The diagnosis was made solely on the basis of incisional biopsy, transbronchial lung biopsy/bronchoalveolar lavage, or surgical excision and was determined on hematoxylin and eosin- and Giemsa-stained preparations, supported by inmmunohistochemical analysis. For staging, the Ann Arbor system³¹ was used; all patients were human immunodeficiency virus–negative.

The staging evaluation included initial hematologic and chemical surveys and a physical examination, in addition to chest radiographs and computed tomography of the chest and abdomen, abdominal ultrasonography, and gastroduodenoscopy. A bone marrow biopsy and an otorhinolaryngologic examination were performed in all patients. Patients with a conjunctival site underwent a complete ophthalmic examination, including double eversion of the upper eyelids to examine the upper fornix.

Therapeutic Approaches
Patients were treated according to disease stage and site. Patients with localized lymphoma generally were treated with surgery or local radiation therapy, whereas other patients received adjuvant chemotherapy. Advanced-stage patients were given chemotherapy, either as a single-agent regimen (chlorambucil, cyclophosphamide, or fludarabine) or as a polychemotherapy regimen (cyclophosphamide, doxorubicin, vincristine, and prednisone [CHOP]; CHOP-like regimen; or etoposide, mitoxantrone, cyclophosphamide, vincristine, prednisone, and bleomycin³²). In addition, in four patients with a conjunctival site and one patient with lachrymal involvement, therapy was restricted to local intralesional administration of interferon alfa-2a (IFN2a) (3 MU three times/week) for 4 to 6 weeks.

Response Criteria
Complete response (CR) was defined as the complete absence for at least 6 weeks of all clinical evidence of the lymphoma; reduction of at least 50% of known disease for at least 6 weeks was rated as a partial response (PR). Patients with stable or progressive disease were to be considered as having no response. Survival and relapse-free survival curves were calculated according to the method of Kaplan and Meier.³³ The survival curve was measured from diagnosis until death; the time to treatment failure interval was calculated from the end of induction therapy to the first evidence of relapse (for CRs) or to the first evidence of progression (for PRs).

	RESULTS

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION REFERENCES

 
Patient Characteristics
Thirty-five patients were males, and 40 were females (Table 1). Their ages ranged from 27 to 91 years (median, 58 years). The lymphomas were localized to the lung (19 patients), orbital soft tissue (16 patients), skin (seven patients), thyroid (seven patients), lachrymal gland (six patients), conjunctiva (six patients), salivary gland (six patients), breast (three patients), eyelid (two patients), larynx (one patient), bone marrow (one patient), and trachea (one patient). At diagnosis, 47 patients (63%) had stage IE or IIE disease, and 28 patients (37%) had advanced-stage disease. Thirteen patients had bone marrow involvement. Eight patients (11%) were hepatitis C-positive; in these patients, the disease was localized to the lung (two patients), orbital soft tissue (one patient), skin (one patient), salivary glands (one patient), lachrymal gland (one patient), and larynx (one patient). One case manifested in the eyelid but was accompanied by bone marrow involvement. As regards the correlation with autoimmune diseases, one (14%) of seven patients with thyroid lymphoma had previous Hashimoto's thyroiditis, and one (17%) of six patients with lachrymal gland lymphoma had previous Sjögren's disease.

Of the 75 patients, 59 (79%) achieved a CR, and the remaining 16 (21%) achieved a PR. Among stage IE and IIE patients, 41 (87%) of 47 patients obtained a CR and six (13%) had a PR, whereas among the 28 advanced-stage patients, 18 (64%) achieved a CR, and 10 (36%) had a PR. At present, 52 (88%) of 59 patients are still in CR, with a median follow-up of 42 months (range, 8 to 126 months). Three of them are in a second CR after relapses at 12, 41, and 42 months. All but two of the patients are still alive, with a median follow-up of 47 months (range, 8 to 126 months). One patient died of colon carcinoma (orbital soft tissue localization in CR) after 43 months, and one died of gastric hemorrhage (lachrymal gland localization in PR) after 35 months. Figure 1 depicts the estimated time to treatment failure of all 75 patients (30% at 5 years) and the estimated overall survival of all 75 patients (95% at 5 years). Figure 2 shows the time to treatment failure curves with respect to stage IE-IIE versus advanced stages (29% for early stages and 32% for advanced stages at 5 years).

View larger version (10K): [in this window] [in a new window]   Fig 1. Overall survival (OS) curve and time to treatment failure (TTF) curve of all 75 patients.

View larger version (9K): [in this window] [in a new window]   Fig 2. Time to treatment failure curves for stage IE-IIE versus stage IV.

Specific Sites: Treatment and Response
Pulmonary lymphoma. Among these 19 patients, 14 received chemotherapy alone, two had surgery plus chemotherapy, two had surgery alone, and the remaining patient had chemotherapy followed by radiation therapy. Fifteen patients (79%) obtained a CR, and four patients (21%) had a PR.

Orbital soft tissue lymphoma. Of these 16 patients, 11 received chemotherapy alone, three had local radiotherapy, and two had chemotherapy plus radiation therapy. Twelve patients (75%) obtained a CR, and four patients (25%) had a PR.

Skin lymphoma. Initial surgery was performed in all seven patients, after which six patients received chemotherapy, and one had local radiation therapy. Five patients (72%) obtained a CR, and two patients (28%) had a PR.

Thyroid lymphoma. All seven patients received local excision followed by chemotherapy, either alone (five patients) or in association with local radiotherapy (two patients). All patients (100%) obtained a CR.

Lachrymal gland lymphoma. Among these six patients, two received surgery alone, two had surgery followed by chemotherapy, one received chemotherapy alone, and the remaining patient had local IFN2a alone. Among these patients, four (67%) obtained a CR, and two (33%) had a PR.

Conjunctival lymphoma. These six patients received either local administration of IFN2a alone (four patients) or surgery alone (two patients). All four patients treated with IFN2a obtained a CR (67%), whereas the two patients who received surgery alone (33%) had a PR.

Salivary gland lymphoma. All six patients received chemotherapy, and two of them also had local radiation therapy. CR was achieved by four patients (67%), and two patients (33%) had a PR.

Other sites. All patients who presented with involvement at other sites achieved a CR: breast (three patients with local excision plus chemotherapy), eyelid (two patients; one with local radiation therapy and one with surgical treatment), larynx (one patient with local radiation therapy), bone marrow (one patient with chemotherapy), and trachea (one patient with local radiotherapy).

Bone marrow involvement. Twelve patients (16%) (three with pulmonary, three with salivary gland, two with lachrymal gland, two with orbital soft tissue, and two with conjunctival sites) also presented with contemporary involvement of the bone marrow. Four (34%) of these patients achieved a CR and have continued to maintain the response, whereas all of the remaining patients obtained a PR with minimal residual disease in the bone marrow.

Localized versus advanced disease. Among the 47 stage I-II patients, the CR rate was 87%, whereas in the 28 patients with advanced disease (stage IV), the CR rate was 64%. Therapy, which was selected independently of stage, was based on the specific site of MALT and on the tumor burden.

Relapse Pattern: Sites of Lymphoma
Among the 10 patients who relapsed, there were three patients with pulmonary lymphoma, two with orbital soft tissue involvement, two with skin lymphoma, one with conjunctival involvement, one with salivary gland lymphoma, and one with breast lymphoma. The pattern of relapses was characterized by seven local recurrences (in the vicinity of the removed tumor) and three relapses at other sites; all were histologically documented as low-grade MALT lymphoma. The three recurrences distant from the primary site were represented by breast and contralateral breast, salivary gland and other lymph nodes of the neck, and orbital soft tissue and further skin relapse. Three of the 10 patients obtained a second CR: in particular, two with recurrence at another site (breast-contralateral breast and orbital soft tissue-skin) and one with local relapse (eyelid); these three patients are still alive and disease-free at 36, 16, and 13 months after their second treatment responses. The remaining patients obtained a PR after the re-treatment; all are currently alive with disease.

Figure 3 depicts the time to treatment failure curves with respect to the five main lymphoma sites. No relapses/progressions were observed in the thyroid subgroup. Because of the low number of patients, no statistically significant difference was observed among the different sites.

View larger version (12K): [in this window] [in a new window]   Fig 3. Time to treatment failure curves for the five main sites.

	DISCUSSION

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION REFERENCES

 
Although as many as 60% of all MALT lymphomas occur in the gastrointestinal tract (especially the stomach), where MALT normally occurs, the tumor often involves nonmucosal epithelia (eg, salivary gland, thyroid, conjunctiva, breast) or mucosal sites without a significant amount of normal lymphoid tissue (eg, lung), or, occasionally, nonepithelial tissues (eg, orbital soft tissue). The nongastrointestinal sites most frequently involved by MALT lymphomas are the lung and orbital soft tissue.

Regarding the clinical characteristics of the disease, our data confirm the specific features of nongastrointestinal MALT lymphoma outlined in the previous reports by Thieblemont et al³⁴ and Zinzani et al.³⁵ In particular, in the patients of the present series, there was a predominance of female patients with a median age of 55 to 60 years, and the lung and orbital soft tissue were the most frequent sites. Among our MALT lymphomas, the correlation with autoimmune disease seems to have been less strong than in other types of lymphoma. In the current study, there was a CR rate of 79% and an overall response rate of 100%. With respect to the specific sites, all seven thyroid lymphoma patients (100%) obtained a CR, whereas patients with involvement at other sites at which at least six patients were affected (lung, orbital soft tissue, skin, lachrymal gland, conjunctiva, and salivary gland) had CR rates ranging from 67% to 79%. A particularly poor response was encountered among those patients with concomitant mucosal and bone marrow involvement,³⁶ who had a CR rate of only 34%.

Among the 59 CRs, only 10 relapses (17%) were observed. Overall, the time to treatment failure rate was 30% at 5 years; in particular, the thyroid subset had the best time to treatment failure rate (Fig 3). After a median follow-up of 47 months (range, 8 to 126 months), overall survival is 95%. Relapses occurred as local recurrences, dissemination to other organs, or in different locations of the same extranodal site. One third of the relapsed patients obtained a second CR, and all of the relapses have shown at least a PR with a good outcome.

The therapeutic approach was evaluated in relation to the different organs involved. In particular, chemotherapy was most effective for lung disease, whereas surgical excision and radiotherapy or local IFN2a were preferred for the orbital soft tissue and conjunctiva, respectively. It should be emphasized that the local intralesional administration of IFN2a for conjunctival and lachrymal gland sites proved effective, with all five patients achieving a CR without relapse with this treatment alone.

To the best of our knowledge, this is the largest reported series to date of nongastrointestinal MALT lymphomas. Our data confirm that the prognosis of this particular entity is more favorable than that of other extranodal lymphomas. However, several aspects await clarification, such as the issues of homing receptors and the antigenic dependency of the lymphoma. With regard to the specific therapeutic approaches, our data support the effectiveness of combination therapy (chemotherapy plus radiation therapy) in the majority of sites, the effectiveness of local treatment with IFN2a in particular sites where radiation therapy could be the cause of unpleasant and dangerous sequelae, and the role of chemotherapy (using CHOP or CHOP-like regimens) in the lung. Nevertheless, no firm conclusions can be drawn regarding the most appropriate treatment with respect to the stage of the lymphoma. In fact, for MALT lymphoma patients, the therapeutic approaches have to be tailored according to the specific site, and this makes it extremely difficult to stratify the different early- and advanced-stage treatments. In terms of response duration, the thyroid and lachrymal gland sites seem to represent the best subgroups, whereas the skin presents a poorer outcome. The demonstrated possibility of achieving good results and long-lasting survival in all patients by means of differentiated therapeutic approaches in accordance with the particular extranodal site underlines the importance of correctly identifying nongastrointestinal MALT lymphomas.

	REFERENCES

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION REFERENCES

 
1. Isaacson P, Wright DH: Malignant lymphoma of mucosa associated lymphoid tissue: A distinctive type of B-cell lymphoma. Cancer 52:1410-1416, 1983[Medline]

2. Kaplan MA, Pettit CL, Zukerberg LR, et al: Primary lymphoma of the trachea with morphologic and immunophenotypic characteristics of low-grade B-cell lymphoma mucosa-associated lymphoid tissue. Am J Surg Pathol 16:71-75, 1992[Medline]

3. Poletti V, Romagna M, Gasponi A, et al: Bronchoalveolar lavage in the diagnosis of low-grade, MALT type, B-cell lymphoma in the lung. Monaldi Arch Chest Dis 50:191-194, 1995[Medline]

4. Fiche M, Capron F, Berger F, et al: Primary pulmonary non-Hodgkin's lymphomas. Histopathology 26:529-537, 1995[Medline]

5. Nicholson AG, Wotherspoon AC, Diss TC, et al: Pulmonary B-cell non-Hodgkin's lymphomas: The value of immunohistochemistry and gene analysis in diagnosis. Histopathology 26:395-403, 1995[Medline]

6. Hyjek E, Smith WJ, Isaacson PG: Primary B cell lymphoma of salivary glands and its relationship to myepithelial sialadenitis. Hum Pathol 19:766-776, 1988[Medline]

7. Nair PNP, Schroeder HE: Duct-associated lymphoid tissue (DALT) of minor salivary glands and mucosal immunity. Immunology 57:171-180, 1986[Medline]

8. Hyjek E, Isaacson PG: Primary B cell lymphoma of the thyroid and its relationship to Hashimoto's thyroiditis. Hum Pathol 19:1315-1326, 1988[Medline]

9. Isaacson PG, Chan JKC, Tang C, et al: Low-grade B-cell lymphoma of mucosa-associated lymphoid tissue arising in the thymus: A thymic lymphoma mimicking myoepithelial sialadenitis. Am J Surg Pathol 14:342-351, 1990[Medline]

10. Mattia AR, Ferry JA, Harris NL: Breast lymphoma: A B-cell spectrum including the low grade B-cell lymphoma of mucosa associated lymphoid tissue. Am J Surg Pathol 17:574-587, 1993[Medline]

11. Slater DN: MALT and SALT: The clue to cutaneous B-cell lymphoproliferative disease. Br J Dermatol 131:557-561, 1994[Medline]

12. Bailey EM, Ferry JA, Harris NL, et al: Marginal zone lymphoma (low-grade B-cell lymphoma of mucosa-associated lymphoid tissue type) of skin and subcutaneous tissue. Am J Surg Pathol 20:1011-1023, 1996[Medline]

13. Isaacson PG, Banks PM, Best PV, et al: Primary low-grade hepatic B-cell lymphoma of mucosa-associated lymphoid tissue (MALT)-type. Am J Surg Pathol 19:571-575, 1995[Medline]

14. Wotherspoon AC, Hardman-Lea S, Isaacson PG: Mucosa-associated lymphoid tissue (MALT) in the human conjunctiva. J Pathol 174:33-37, 1994[Medline]

15. Hardman-Lea S, Kerr-Muir M, Wotherspoon AC, et al: Mucosal-associated lymphoid tissue lymphoma of the conjunctiva. Arch Ophthalmol 112:1207-1212, 1994[Abstract]

16. Polito E, Leccisotti A: Prognosis of orbital lymphoid hyperplasia. Graefes Arch Clin Exp Ophthalmol 230:150-154, 1996

17. Polito E, Galieni P, Leccisotti A: Clinical and radiological presentation of 95 orbital lymphoid tumors. Graefes Arch Clin Exp Ophthalmol 234:504-509, 1996[Medline]

18. Calvo R, Ribera JM, Vaquero M, et al: Low-grade, MALT-type, primary B-cell lymphoma of the conjunctiva. Leuk Lymphoma 28:203-207, 1997[Medline]

19. The Non-Hodgkin's Lymphoma Pathologic Classification Project: National Cancer Institute sponsored study of classifications of non-Hodgkin's lymphomas: Summary and description of a Working Formulation for Clinical Usage. Cancer 49:2112-2135, 1982[Medline]

20. Lennert K, Feller AC: Histopathologie der Non-Hodgkin Lymphome (nach der acktulisierten Kiel-Klassifikation). Berlin, Germany, Springer-Verlag, 1990

21. Harris NL, Jaffe ES, Stein H, et al: A revised European-American classification of lymphoid neoplasms: A proposal from the International Lymphoma Study Group. Blood 84:1361-1392, 1994[Free Full Text]

22. Wotherspoon AC, Ortiz-Hidalgo C, Falzon MR, et al: Helicobacter pylori-associated gastritis and primary B-cell gastric lymphoma. Lancet 338:1175-1176, 1991[Medline]

23. Wotherspoon AC, Doglioni C, Diss TC, et al: Regression of primary low-grade B cell gastric lymphoma of mucosa associated lymphoid type after eradication of Helicobacter pylori. Lancet 342:575-577, 1993[Medline]

24. Nicholson AG, Wotherspoon AC, Jones AL, et al: Pulmonary B-cell non-Hodgkin's lymphoma associated with autoimmune disorders: A clinicopathological review of six cases. Eur Respir J 9:2022-2025, 1996[Abstract]

25. Isaacson PG: Lymphomas of mucosa-associated lymphoid tissue (MALT). Histopathology 76:617-619, 1990

26. Isaacson PG: Extranodal lymphomas: The MALT concept. Verh Dtsch Ges Pathol 76:14-23, 1992[Medline]

27. Neri A, Jacobiec FA, Pelicci PG, et al: Immunoglobulin and T cell receptor beta chain gene rearrangement analysis of ocular adnexal lymphoid neoplasms: Clinical and biologic implications. Blood 70:1519-1529, 1987[Abstract/Free Full Text]

28. Luppi M, Longo G, Ferrari MG, et al: Additional neoplasms and HCV infection in low-grade lymphoma of MALT type. Br J Haematol 94:373-375, 1996[Medline]

29. Ascoli V, Lo Coco F, Artini M, et al: Extranodal lymphomas associated with hepatitis C virus infection. Am J Clin Pathol 109:600-609, 1998[Medline]

30. Tkoub EM, Haioun C, Pawlotsky JM, et al: Chronic hepatitis C virus and gastric MALT lymphoma. Blood 91:360, 1998 (letter)[Free Full Text]

31. Carbone PP, Kaplan HS, Musshoff K, et al: Report of the committee on Hodgkin's disease staging classifications. Cancer 31:1860-1861, 1971

32. Zinzani PL, Pavone E, Storti S, et al: Randomized trial with or without granulocyte colony-stimulating factor as adjunct to induction VNCOP-B treatment of elderly high-grade non-Hodgkin's lymphoma. Blood 89:3974-3979, 1997[Abstract/Free Full Text]

33. Kaplan EL, Meier P: Nonparametric estimation from incomplete observations. J Am Stat Assoc 53:457-481, 1958

34. Thieblemont C, Bastion Y, Berger F, et al: Mucosa-associated lymphoid tissue gastrointestinal and nongastrointestinal lymphoma behavior: Analysis of 108 patients. J Clin Oncol 15:1624-1630, 1997[Abstract]

35. Zinzani PL, Magagnoli M, Ascani S, et al: Nongastrointestinal mucosa-associated lymphoid tissue (MALT) lymphomas: Clinical and therapeutic features of 24 localized patients. Ann Oncol 8:883-886, 1997[Abstract/Free Full Text]

36. Graziadei G, Pruneri G, Carboni N, et al: Low-grade MALT lymphoma involving multiple mucosal sites and bone marrow. Ann Hematol 76:81-83, 1998[Medline]

Submitted July 2, 1998; accepted December 17, 1998.

This article has been cited by other articles:

				U. Vinatzer, M. Gollinger, L. Mullauer, M. Raderer, A. Chott, and B. Streubel Mucosa-Associated Lymphoid Tissue Lymphoma: Novel Translocations Including Rearrangements of ODZ2, JMJD2C, and CNN3 Clin. Cancer Res., October 15, 2008; 14(20): 6426 - 6431. [Abstract] [Full Text] [PDF]

				M. Troch, S. Woehrer, B. Streubel, M. Weissel, M. Hoffmann, L. Mullauer, A. Chott, and M. Raderer Chronic autoimmune thyroiditis (Hashimoto's thyroiditis) in patients with MALT lymphoma Ann. Onc., July 1, 2008; 19(7): 1336 - 1339. [Abstract] [Full Text] [PDF]

				G. Papaxoinis, G. Fountzilas, D. Rontogianni, M. A. Dimopoulos, N. Pavlidis, C. Tsatalas, D. Pectasides, N. Xiros, and T. Economopoulos Low-grade mucosa-associated lymphoid tissue lymphoma: a retrospective analysis of 97 patients by the Hellenic Cooperative Oncology Group (HeCOG) Ann. Onc., April 1, 2008; 19(4): 780 - 786. [Abstract] [Full Text] [PDF]

				J. P. de Boer, R. F. Hiddink, M. Raderer, N. Antonini, B. M. P. Aleman, H. Boot, and D. de Jong Dissemination patterns in non-gastric MALT lymphoma Haematologica, February 1, 2008; 93(2): 201 - 206. [Abstract] [Full Text] [PDF]

				D. Coon, S. Beriwal, S. H. Swerdlow, and R. Bhargava Mucosa-Associated Lymphoid Tissue Lymphoma of the Cervix J. Clin. Oncol., January 20, 2008; 26(3): 503 - 504. [Full Text] [PDF]

				R. J. Korst Primary Lymphoma of the Subglottic Airway in a Patient With Sjogren's Syndrome Mimicking High Laryngotracheal Stenosis Ann. Thorac. Surg., November 1, 2007; 84(5): 1756 - 1758. [Abstract] [Full Text] [PDF]

				C. M Bacon, M.-Q. Du, and A. Dogan Mucosa-associated lymphoid tissue (MALT) lymphoma: a practical guide for pathologists J. Clin. Pathol., April 1, 2007; 60(4): 361 - 372. [Abstract] [Full Text] [PDF]

				L Arcaini, S Burcheri, A Rossi, M Paulli, R Bruno, F Passamonti, E Brusamolino, A Molteni, A Pulsoni, M. Cox, et al. Prevalence of HCV infection in nongastric marginal zone B-cell lymphoma of MALT Ann. Onc., February 1, 2007; 18(2): 346 - 350. [Abstract] [Full Text] [PDF]

				H Narimatsu, Y Ota, M Kami, K Takeuchi, R Suzuki, K Matsuo, T Matsumura, K Yuji, Y Kishi, T Hamaki, et al. Clinicopathological features of pyothorax-associated lymphoma; a retrospective survey involving 98 patients Ann. Onc., January 1, 2007; 18(1): 122 - 128. [Abstract] [Full Text] [PDF]

				S. M. Cohen, M. Petryk, M. Varma, P. S. Kozuch, E. D. Ames, and M. L. Grossbard Non-Hodgkin's Lymphoma of Mucosa-Associated Lymphoid Tissue Oncologist, November 1, 2006; 11(10): 1100 - 1117. [Abstract] [Full Text] [PDF]

				F. M. Iwamoto, L. M. DeAngelis, and L. E. Abrey Primary dural lymphomas: A clinicopathologic study of treatment and outcome in eight patients Neurology, June 13, 2006; 66(11): 1763 - 1765. [Abstract] [Full Text] [PDF]

				L. Arcaini, S. Burcheri, A. Rossi, F. Passamonti, M. Paulli, E. Boveri, E. Brusamolino, E. Orlandi, A. Molteni, A. Pulsoni, et al. Nongastric Marginal-Zone B-Cell MALT Lymphoma: Prognostic Value of Disease Dissemination. Oncologist, March 1, 2006; 11(3): 285 - 291. [Abstract] [Full Text] [PDF]

				V. Sankaranarayanan, T. M. Zeidalski, and R. K. Chitkara A 55-Year-Old Smoker With a Persistent Right Lower Lobe Infiltrate Chest, June 1, 2005; 127(6): 2266 - 2270. [Full Text] [PDF]

				K Okubo, N Miyamoto, and C Komaki Primary mucosa-associated lymphoid tissue (MALT) lymphoma of the trachea: a case of surgical resection and long term survival Thorax, January 1, 2005; 60(1): 82 - 83. [Abstract] [Full Text] [PDF]

				M. Bendandi, S. A. Pileri, and P. L. Zinzani Challenging paradigms in lymphoma treatment Ann. Onc., May 1, 2004; 15(5): 703 - 711. [Full Text] [PDF]

				S. Wohrer, J. Drach, M. Hejna, W. Scheithauer, A. Dirisamer, A. Puspok, A. Chott, and M. Raderer Treatment of extranodal marginal zone B-cell lymphoma of mucosa-associated lymphoid tissue (MALT lymphoma) with mitoxantrone, chlorambucil and prednisone (MCP) Ann. Onc., December 1, 2003; 14(12): 1758 - 1761. [Abstract] [Full Text] [PDF]

				R. W. Tsang, M. K. Gospodarowicz, M. Pintilie, W. Wells, D. C. Hodgson, A. Sun, M. Crump, and B. J. Patterson Localized Mucosa-Associated Lymphoid Tissue Lymphoma Treated With Radiation Therapy Has Excellent Clinical Outcome J. Clin. Oncol., November 15, 2003; 21(22): 4157 - 4164. [Abstract] [Full Text] [PDF]

				A. Conconi, G. Martinelli, C. Thieblemont, A. J. M. Ferreri, L. Devizzi, F. Peccatori, M. Ponzoni, E. Pedrinis, S. Dell'Oro, G. Pruneri, et al. Clinical activity of rituximab in extranodal marginal zone B-cell lymphoma of MALT type Blood, October 15, 2003; 102(8): 2741 - 2745. [Abstract] [Full Text] [PDF]

				E. Zucca, A. Conconi, E. Pedrinis, S. Cortelazzo, T. Motta, M. K. Gospodarowicz, B. J. Patterson, A. J. M. Ferreri, M. Ponzoni, L. Devizzi, et al. Nongastric marginal zone B-cell lymphoma of mucosa-associated lymphoid tissue Blood, April 1, 2003; 101(7): 2489 - 2495. [Abstract] [Full Text] [PDF]

				B. Streubel, A. Lamprecht, J. Dierlamm, L. Cerroni, M. Stolte, G. Ott, M. Raderer, and A. Chott T(14;18)(q32;q21) involving IGH and MALT1 is a frequent chromosomal aberration in MALT lymphoma Blood, March 15, 2003; 101(6): 2335 - 2339. [Abstract] [Full Text] [PDF]

				J. Cadranel, M. Wislez, and M. Antoine Primary pulmonary lymphoma Eur. Respir. J., September 1, 2002; 20(3): 750 - 762. [Abstract] [Full Text] [PDF]

				F. Cavalli, P. G. Isaacson, R. D. Gascoyne, and E. Zucca MALT Lymphomas Hematology, January 1, 2001; 2001(1): 241 - 258. [Abstract] [Full Text] [PDF]

				C. Thieblemont, F. Berger, C. Dumontet, I. Moullet, F. Bouafia, P. Felman, G. Salles, and B. Coiffier Mucosa-associated lymphoid tissue lymphoma is a disseminated disease in one third of 158 patients analyzed Blood, February 1, 2000; 95(3): 802 - 806. [Abstract] [Full Text] [PDF]

This Article Abstract Full Text (PDF) Purchase Article View Shopping Cart Alert me when this article is cited Alert me if a correction is posted Services Email this article to a colleague Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Save to my personal folders Download to citation manager Rights & Permissions Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Zinzani, P. L. Articles by Tura, S. Search for Related Content PubMed PubMed Citation Articles by Zinzani, P. L. Articles by Tura, S.