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Marginal Zone B-Cell Lymphoma: A Clinical Comparison of Nodal and Mucosa-Associated Lymphoid Tissue Types

From the University of Southern California (USC) and Los Angeles County+USC Healthcare Network, Los Angeles, CA; University of Nebraska Medical Center, Omaha, NE; Ospedale San Giovanni, Bellinzona, Switzerland; Hotel Dieu de Paris, Paris, France; Harvard Medical School, Boston, MA; St James University, Leeds, United Kingdom; and University of Würzburg, Würzburg, Germany.

Address reprint requests to Bharat N. Nathwani, MD, Los Angeles County–University of Southern California Healthcare Network, General Hospital, Rm 2422, 1200 North State St, Los Angeles, CA 90033.

	ABSTRACT

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION APPENDIX REFERENCES

 
PURPOSE: In the International Lymphoma Study Group classification of lymphoma, extranodal marginal zone B-cell lymphoma (MZL) of mucosa-associated lymphoid tissue (MALT) type is listed as a distinctive entity. However, nodal MZL is listed as a provisional entity because of questions as to whether it is truly a disease or just an advanced stage of MALT-type MZL. To resolve the issue of whether primary nodal MZL without involvement of mucosal sites exists and whether it is clinically different from extranodal MALT-type lymphoma, we compared the clinical features of these two lymphomas.

PATIENTS AND METHODS: Five expert hematopathologists reached a consensus diagnosis of MZL in 93 patients. Seventy-three were classified as having MALT-type MZL because of involvement of a mucosal site at the time of diagnosis, and 20 were classified as having nodal MZL because of involvement of lymph nodes without involvement of a mucosal site.

RESULTS: A comparison of the clinical features of nodal MZL and MALT-type MZL showed that more patients with nodal MZL presented with advanced-stage disease (71% v 34%; P = .02), peripheral lymphadenopathy (100% v 8%; P < .001), and para-aortic lymphadenopathy (56% v 14%; P < .001) than those with MALT-type MZL. However, fewer patients with nodal MZL had a large mass ( 5 cm) than those with MALT-type MZL (31% v 68%; P = .03). The 5-year overall survival of patients with nodal MZL was lower than that for patients with MALT-type MZL (56% v 81%; P = .09), with a similar result for failure-free survival (28% v 65%; P = .01). Comparisons of patients with International Prognostic Index scores of 0 to 3 showed that those with nodal MZL had lower 5-year overall survival (52% v 88%; P = .025) and failure-free survival (30% v 75%; P = .007) rates than those with MALT-type MZL.

CONCLUSION: Nodal MZL seems to be a distinctive disease entity rather than an advanced stage of MALT-type MZL because the clinical presentations and survival outcomes are different in these two types of MZL. Clinically, nodal MZL is similar to other low-grade, node-based B-cell lymphomas, such as follicular and small lymphocytic lymphomas.

	INTRODUCTION

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION APPENDIX REFERENCES

 
IN 1983, ISAACSON AND Wright^1,2 reported a new lymphoma under the heading of extranodal malignant lymphoma arising from mucosa-associated lymphoid tissue (MALT), which over the next 10 years came to be known as MALT lymphoma. Since the original publication in 1983, numerous studies have established that extranodal MALT-type lymphoma is a distinctive clinicopathologic entity.^3-13 Patients with this lymphoma usually have localized disease, an indolent natural history, and long survival.^3-13 Involvement of regional lymph nodes is observed in a minority of the patients at the time of diagnosis, or it may occur years after the diagnosis.^{4-6,8-10,13,14} Moreover, histologic progression to a diffuse large B-cell lymphoma occurs frequently in MALT-type lymphoma.^{4-6,8-10,12,13} In 1994, the International Lymphoma Study Group (ILSG) proposal called this lymphoma extranodal marginal zone B-cell lymphoma (MZL) of MALT type.¹⁵

Since 1986, several publications have used the term monocytoid B-cell lymphoma (MBCL) for lymphomas that contain malignant monocytoid B cells, regardless of whether they involve nodal and/or extranodal sites.^16-28 In some of these reports, primary nodal cases of MBCL were in the minority. In 1994, nodal MBCL was listed in the ILSG proposal as a provisional entity and designated as nodal MZL.¹⁵ This was considered a provisional entity because in many of the reported cases of MBCL, there was also involvement of an extranodal site, and such cases, according to the ILSG definition, would be called MALT-type lymphoma (advanced stage) and not nodal MZL.

A large-scale review of an international group of lymphomas was undertaken to determine whether the entities defined in the ILSG classification were clinically distinctive.²⁹ To resolve the issue of whether primary nodal MZL without involvement of mucosal sites exists and whether it is clinically different from extranodal MALT-type lymphoma, we compared these two lymphomas with respect to: (1) the clinical findings at presentation; (2) sites of involvement at presentation; (3) overall survival and failure-free survival; and (4) the frequency of associated diffuse large B-cell lymphoma.

	PATIENTS AND METHODS

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION APPENDIX REFERENCES

 
The details of the materials and methods used in this study were recently published.²⁹ Briefly, a consecutive cohort of 1,378 previously untreated cases of non-Hodgkin's lymphoma diagnosed between January 1988 and December 1990 at nine different centers in eight countries was evaluated individually by five expert hematopathologists. The results reported in this study are the consensus diagnoses of the five pathologists.

The criteria used by the five pathologists in this study were those proposed by the ILSG.¹⁵ As long as a case had involvement of a mucosal or other extranodal nonhematopoietic site by low-grade MZL, it was classified as extranodal MZL of MALT type, regardless of whether other sites were involved. A case was classified as nodal MZL if a lymph node was involved by MZL and there was no evidence of involvement of an extranodal MALT site. On the basis of these definitions, two groups (MALT-type MZL and nodal MZL) were created. Patients whose histologic material also contained many large B cells were classified as having MZL plus diffuse large B-cell lymphoma. Then, nodal MZL and MALT-type MZL were compared with respect to age, stage, "B" symptoms, serum lactate dehydrogenase level, a mass 5 cm at diagnosis, bone marrow involvement, International Prognostic Index (IPI) scores,³⁰ overall and failure-free survival rates, and the frequency of associated diffuse large B-cell lymphoma. In some cases, information on one or more of these clinical parameters was not available. Failure-free survival was defined as the time from diagnosis to the first occurrence of progression, relapse after response, or death from any cause. Follow-up of patients who did not experience one of these events was censored at the date of last contact. Overall survival was measured from diagnosis to death from any cause, with surviving patient follow-up censored at the last contact date. Estimates of overall and failure-free survival distribution were calculated using the method of Kaplan and Meier.³¹ Time to event distributions were compared using the log-rank test.³²

	RESULTS

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION APPENDIX REFERENCES

 
Comparison of the Clinical Findings at Presentation
The consensus diagnosis of the five pathologists was extranodal MZL of MALT type for 73 patients and nodal MZL for 20 patients, with all of the latter cases characterized by monocytoid B cells. A comparison of the clinical findings at the time of initial diagnosis is shown in Table 1. A significantly higher percentage of patients with nodal MZL had advanced-stage (III and IV) disease than did patients with MALT-type MZL (71% v 34%; P = .02). Patients with nodal MZL were also more likely to have bone marrow involvement than those with MALT-type MZL, although the difference between the two groups was not statistically significant. A significantly lower proportion of patients with nodal MZL had a mass 5 cm than did patients with MALT-type MZL (31% v 68%; P = .03). No other statistically significant differences were found.

Comparison of the Distribution of Disease at Presentation
All cases of MALT-type MZL had involvement of one or more extranodal MALT sites (Table 2). The most common site of involvement was the stomach. There were significant differences in the distribution of disease between MALT-type MZL and nodal MZL (Table 3). The major difference was in the occurrence of peripheral lymphadenopathy, which was found in every patient with nodal MZL but in only five patients with MALT-type MZL (100% v 8%; P < .001). Three of these five patients had concomitant involvement of an adjacent MALT site; in the remaining two patients, lymph nodes distant from the extranodal sites were involved. No patient with MALT-type MZL had inguinal or femoral lymph node involvement, and only one patient had axillary lymph node involvement. In contrast, in nodal MZL, inguinal and/or femoral lymph nodes were involved in 63% (P < .001) and axillary nodes in 44% (P < .001) of the patients. Para-aortic lymphadenopathy was also found in a significantly higher proportion of patients with nodal MZL than in those with MALT-type MZL (56% v 14%; P < .001). The frequency of involvement of the bone marrow, spleen, and liver was also higher in nodal MZL than in MALT-type MZL, but these differences did not reach statistical significance.

Comparison of Survival
Information on survival was available for 62 patients with MALT-type MZL and 14 patients with nodal MZL. The 5-year overall survival rate for patients with nodal MZL was lower than for those with MALT-type MZL (Fig 1; 56% v 81%; P = .09), and the 5-year failure-free survival rate for nodal MZL was significantly lower than for MALT-type MZL (Fig 2; 28% v 65%; P = .01). To ascertain the influence of the IPI on survival, we compared patients with IPI scores of 0 to 3 in these two groups. Similarly, we found that the 5-year overall survival rate for nodal MZ was significantly lower than that for MALT-type MZL (Fig 3; 52% v 88%; P = .025), with similar results for 5-year failure-free survival (Fig 4; 30% v 75%; P = .007).

View larger version (13K): [in this window] [in a new window]   Fig 1. Patients with MALT-type MZL had a longer overall survival duration than those with nodal MZL (P = .09).

View larger version (14K): [in this window] [in a new window]   Fig 2. Patients with MALT-type MZL had a significantly longer failure-free survival duration than those with nodal MZL (P = .01).

View larger version (13K): [in this window] [in a new window]   Fig 3. The overall survival duration of patients with MALT-type MZL who had an IPI score of 0 to 3 was significantly longer than that of those with nodal MZL (P = .025).

View larger version (14K): [in this window] [in a new window]   Fig 4. The failure-free survival duration of patients with MALT-type MZL who had an IPI score of 0 to 3 was significantly longer than that of those with nodal MZL (P = .007).

Comparison of Frequency of Associated Diffuse Large B-cell Lymphoma
The consensus diagnosis was MALT-type lymphoma in 73 patients and MALT-type MZL plus diffuse large B-cell lymphoma in 32 additional patients, indicative of transformation. Thus, for every two patients with MALT-type MZL, one showed evidence of histologic progression at diagnosis (ratio of 2.3:1 or a frequency of 30% [32 of 105]). In contrast, there were 20 cases of nodal MZL and five additional cases of nodal MZL plus diffuse large B-cell lymphoma. Thus, for every four patients with nodal MZL, only one showed histologic progression (ratio of 4:1 or a frequency of 20% [five of 25]).

	DISCUSSION

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION APPENDIX REFERENCES

 
A clinical hallmark of MALT-type MZL is that the disease is localized at an extranodal site for a long period of time.^3-13 Clinical spread of MALT-type MZL usually occurs by involvement of local draining lymph nodes or sometimes distant nodes, and occasionally other hematopoietic sites, such as the bone marrow, liver, or spleen.^3-14 Clinical progression also often correlates with transformation to a diffuse large B-cell lymphoma (MALT plus diffuse large B-cell lymphoma).^{4-6,8-10,12,13}

There has been debate about whether nodal MZL is different from MALT-type MZL or is merely an advanced stage of MALT-type lymphoma.¹⁵ In this study, using the ILSG criteria for classification,¹⁵ we identified two groups of patients, those with extranodal MALT-type MZL and those with nodal MZL, based on whether the lymphoma involved a primary mucosal site at the time of initial diagnosis. Patients with MALT-type MZL always had involvement of one or more MALT sites, whereas those with nodal MZL by definition lacked involvement of any MALT site, but rather had primary involvement of lymph nodes. These two groups were then compared with respect to their clinical findings and sites of involvement at presentation, their overall and failure-free survival, and the frequency of associated diffuse large B-cell lymphoma.

Our data show that there are important differences in the distribution and extent of disease between nodal MZL and MALT-type MZL. All nodal MZL patients had peripheral lymphadenopathy, whereas it was present in only five patients with MALT-type MZL (P < .001), three of whom had involvement of a nearby MALT site. Thus, the presence of peripheral lymphadenopathy is typical of nodal MZL rather than MALT-type MZL. The presence of para-aortic lymphadenopathy was also much more common in nodal MZL than in MALT-type MZL (P < .001). The frequency of bone marrow, liver, and splenic involvement was also higher in nodal MZL than in MALT-type MZL, but statistical comparisons did not reach significance, perhaps because of the small sample sizes. Thus, the distribution of disease in nodal MZL is similar to that of other primary node-based "low-grade" B-cell lymphomas (follicular, small lymphocytic, lymphoplasmacytic) wherein patients have generalized lymphadenopathy, often with involvement of the bone marrow, liver, and spleen.²⁹ In contrast to nodal MZL, patients with MALT-type MZL present with involvement of MALT sites by a localized mass, and, when lymph nodes are involved, the nodes are usually localized to adjacent draining sites.^3-15,29 The survival data also suggest that nodal MZL is more like other primary nodal low-grade lymphomas and different from MALT-type MZL. For all patients, those with nodal MZL had a shorter overall and failure-free survival durations than did those with MALT-type MZL (Figs 1 and 2). Similar results were found when comparisons were made for patients with IPI scores of 0 to 3 (Figs 3 and 4).

To examine further the validity of whether nodal MZL represents an advanced stage of MALT-type MZL, we also compared the clinical features (Table 1) and the frequency of associated diffuse large B-cell lymphoma (histologic transformation) in these two groups. If nodal MZL were simply an advanced stage of MALT-type MZL, a large tumor mass ( 5 cm) also should have been observed in at least an equal, if not greater, number of patients diagnosed as nodal MZL. However, the reverse was true: a large mass was found in only 31% of patients with nodal MZL, whereas it was observed in 68% of patients with MALT-type MZL (Table 1). In addition, if nodal MZL represents an advanced stage of MALT-type MZL, one would expect patients with nodal MZL to be older and more likely to have B symptoms, an elevated lactate dehydrogenase level, a poor performance status, and more adverse risk factors in the IPI. Although our results show that patients with nodal MZL had widespread disease, all of our other data strongly suggest that nodal MZL is not an advanced stage of MALT-type MZL. Patients with nodal MZL were not older than those with MALT-type MZL, and there was no difference in the frequency of B symptoms, lactate dehydrogenase levels, performance status, and IPI scores (Table 1). In addition, if nodal MZL is an advanced stage of MALT-type MZL, one might have expected a higher incidence of associated diffuse large B-cell lymphoma (histologic transformation) in nodal MZL, but this was not the case (20% for nodal MZL v 30% for MALT-type MZL; P = .25).

In 1995, the Southwest Oncology Group published a study of patients with stages III and IV lymphoma who were treated with cyclophosphamide, doxorubicin, vincristine, and prednisone, wherein 19 patients with MALT-type lymphoma were compared with 21 patients with nodal MZL.²⁸ However, of the 19 patients with MALT-type lymphoma, seven (37%) also had follicular lymphoma and 12 had pure MALT-type lymphoma. Similarly, of the 21 patients with nodal MZL, 13 (62%) also had follicular lymphoma, whereas only eight had pure nodal MZL. In that study, no clinical data, including overall or failure-free survival, were given for the 12 patients with pure MALT-type lymphoma or the eight patients with nodal MZL.²⁸ Therefore, we are not able to compare their data with ours.

In summary, we have shown that there are marked differences in the distribution of disease and clinical behavior between nodal MZL and MALT-type MZL and that these differences are probably a reflection on the inherent biology of these two lymphomas. As the ILSG has suggested, it is likely to be the inherent biology of a disease that dictates its clinical features, natural history, and prognosis.¹⁵ Therefore, nodal MZL should be separated from MALT-type lymphoma and considered a distinctive disease entity, as is proposed in the new World Health Organization classification.³³ However, because all patients with nodal MZL in the present study had monocytoid B cells, it may be appropriate to indicate whether a nodal MZL has monocytoid B cells so that the frequency of nonmonocytoid cases can be ascertained, and it can be determined whether such cases are different from monocytoid nodal MZL.

	APPENDIX

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION APPENDIX REFERENCES

 
Participants in the Non-Hodgkin's Lymphoma Classification Project
Participating pathologists and clinicians at each institution: Wing C. Chan and James O. Armitage, University of Nebraska Medical Center, Omaha, NE; Randy Gascoyne and Joseph Connors, British Columbia Cancer Agency, Vancouver, Canada; Pauline Close and Peter Jacobs, University of Capetown Hospital, Capetown, South Africa; Andrew Norton and T. Andrew Lister, St Bartholomews Hospital, London, United Kingdom; Ennio Pedrinis and Franco Cavalli, Ospedale San Giovanni, Locarno, Switzerland; Francoise Berger and Bertrand Coiffier, Hôpital Edouard-Herriot and Hôpital Sud, Lyon, France; Faith Ho and Raymond Liang, University of Hong Kong, Queen Mary Hospital, Hong Kong; and German Ott, University of Würzburg, Würzburg, and Alfred Schauer and Wolfgang Hiddemann, Georg-August-University Göttingen, Göttingen, Germany.

The five visiting expert hematopathologists who reviewed all cases were: Jacques Diebold, Paris, France; Kenneth A. MacLennan, Leeds, United Kingdom; H. Konrad Müller-Hermelink, Würzburg, Germany; Bharat N. Nathwani, Los Angeles, CA; and Dennis D. Weisenburger, Omaha, NE. Nancy L. Harris, Boston, MA, reviewed slides on 400 cases at two centers. James R. Anderson, Omaha, NE, and Pascal Roy, Lyon, France, provided statistical expertise regarding the study design and data analysis.

	ACKNOWLEDGMENTS

 
Supported in part by United States Public Health Service grant no. CA 36727 awarded by the National Cancer Institute, Department of Health and Human Services, the Foundazione San Salvatore, the Stacey Greene family, and the Imperial Cancer Research Fund, United Kingdom.

	REFERENCES

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Submitted January 11, 1999; accepted April 5, 1999.

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