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Research ArticleClinical Studies

Multi-Database Description of Primary Splenic Diffuse Large B-Cell Lymphoma

KENNETH P. BYRD, NAMRATHA R. VONTELA, BRENNAN MCCULLAR and MIKE G. MARTIN
Anticancer Research December 2017, 37 (12) 6839-6843;
KENNETH P. BYRD
1Department of Hematology/Oncology, University of Tennessee Health Science Center, Memphis, TN, U.S.A.
2The West Cancer Center, Memphis, TN, U.S.A.
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  • For correspondence: kbyrd10@uthsc.edu
NAMRATHA R. VONTELA
1Department of Hematology/Oncology, University of Tennessee Health Science Center, Memphis, TN, U.S.A.
2The West Cancer Center, Memphis, TN, U.S.A.
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BRENNAN MCCULLAR
1Department of Hematology/Oncology, University of Tennessee Health Science Center, Memphis, TN, U.S.A.
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MIKE G. MARTIN
1Department of Hematology/Oncology, University of Tennessee Health Science Center, Memphis, TN, U.S.A.
2The West Cancer Center, Memphis, TN, U.S.A.
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Abstract

Background/Aim: Stage I splenic diffuse large B-cell lymphoma (DLBCL) is rare and there are few data to guide management. We sought to further define prognosis and outcomes. Materials and Methods: We utilized the Surveillance, Epidemiology, and End Results registry to identify patients with stage I splenic DLBCL diagnosed 1973-2013. Patients were divided into two cohorts based on the year of diagnosis (1983-2005; 2006-2013) as rituximab was approved by the U.S. Food and Drug Administration in 2006 for first-line treatment of DLBCL. Results: Utilization of splenectomy decreased after the approval of rituximab (82% pre- versus 72% rituximab-era). Disease-specific and overall survival were greater with splenectomy [hazard ratio (HR)=0.57, p=0.04; and HR=0.66, p=0.03, respectively], but this benefit was only seen in the pre-rituximab cohort, not in the rituximab-era cohort. There was a trend toward improved overall survival with the introduction of rituximab (HR=0.75, p=0.054). Conclusion: Utilization of splenectomy for stage I splenic DLBCL has decreased with the introduction of rituximab without compromising outcomes.

  • Splenic lymphoma
  • large cell lymphoma
  • rituximab
  • Rituxan
  • B-cell lymphoma
  • splenectomy

Primary diffuse large B-cell lymphoma (DLBCL) of the spleen is a rare finding. Originally, Dasgupta et al. defined primary splenic lymphoma (PSL) as being confined to the spleen and hilar nodes (1). Kehoe and Straus modified the definition to include disease that was thought to have started in the spleen or had the bulk of disease confined to the spleen (2). Most studies have selected patients based on the definition of PSL that falls within this spectrum of definitions. The spleen is reported to be involved in 15-40% of all non-Hodgkin's lymphoma, with up to 50-80% involvement at autopsy (3, 4). However, the majority are not considered PSLs. PSL is usually only found in 1-6% of lymphoma cases (3-5). Classically, PSL is most commonly small B-cell lymphoma, such as marginal zone, mantle cell and follicular lymphoma (3, 5, 6). Reports have shown that PSL can also be DLBCL subtype, but less commonly (7-8).

Studies to date suggest that primary splenic DLBCL is not a distinct pathological entity, but just a variation of DLBCL (2, 5). This would suggest that similar treatment guidelines for a more common stage I DLBCL entity could apply to stage I splenic DLBCL. With the U.S. Food and Drug Administration approval of rituximab in 2006, it was incorporated into the standard systemic treatment for stage I DLBCL. Interestingly, studies focused on limited-stage disease (stage I and II) were mostly done in the pre-rituximab era. In 1998, the SWOG 8736 study showed that three cycles of cyclophosphamide, doxorubicin, vincristine, and prednisone (CHOP) plus radiation was superior to eight cycles of CHOP in limited stage (67% stage I) high-grade NHL (9). Since the introduction of rituximab, no randomized controlled trials have focused on the benefit of rituximab in the treatment of limited-stage disease. However, the SWOG 0014 trial showed the progression-free survival benefit of three cycles of rituximab-CHOP (R-CHOP) plus radiation in limited-stage disease compared to historical controls (10). The only randomized trial showing survival benefit of rituximab in DLBCL had very few patients with stage I disease. Interestingly, the original LNH-98.5 study showing survival benefit of R-CHOP versus CHOP in DLBCL only included a single patient with stage I disease (11,12). Subsequent studies have also had an under-representation of stage I disease ranging from 7-20% (13-15).

Overall stage I splenic DLBCL is rare and there are few data to guide management. Potential treatment modalities include combinations of splenectomy, radiation and immunochemotherapy, but there continues to be no consensus on the optimal approach. Splenectomy is the most definitive means of diagnosis, but has certain risks. The complication rate ranges from 6-22% and mortality rate up to 4% (6, 16, 17). Comparatively, a meta-analysis assessing 859 splenic biopsies found the complication rate to be 4% with no deaths (18). Using multiple publicly available and propriety databases, we sought to further define the prognosis and outcomes of stage I splenic DLBCL.

Materials and Methods

We utilized the Surveillance, Epidemiology, and End Results(SEER)18 registry to identify patients with stage I splenic DLBCL diagnosed during the years 1973-2013 using SEER*Stat 8.3.2. Appropriate cases were identified using a combination of International Classification of Diseases for Oncology, 3rd edition code DLBCL (9680/3) and location code for spleen (C42.2) (19). These patients were divided into two cohorts based on the year of diagnosis (1983-2005; 2006-2013) as rituximab was approved by the FDA in 2006 for use in the first-line treatment of DLBCL. Patient characteristics and survival outcomes were analyzed by GraphPad Prism 6 (GraphPad Software, Inc., La Jolla, CA, USA) and Microsoft Excel (Microsoft Corporation, Redmond, WA, USA). Disease-specific (DSS) and overall (OS) survival comparisons were made using the Gehan-Breslow-Wilcoxon test. All p-values were two-sided and results of 0.05 or less were considered significant.

We queried the Mitelman Database of Chromosome Aberrations and Gene Fusions in Cancer to identify patients with stage I splenic lymphoma during the years 1973-2013 (20). We also searched the Caris Life Sciences database for patients profiled by Caris Molecular Intelligence using the key words “splenic lymphoma” in the clinical history and diagnosis fields for cases of stage I splenic DLBCL from 2007-2015 (21). All database searches were conducted with Institutional Review Board approval, #16-04517-XP.

Results

A total of 107,550 patients with known stage and histologically confirmed DLBCL were identified within the SEER database. Out of the 30,455 patients who had stage I disease, only 470 had stage I splenic DLBCL (1.5%). The mean age was 66 years (range=17-93 years) and the majority were Caucasian (89%). There was equal distribution of patients in the pre-rituximab era and post-rituximab era. Overall, 42% (470/1116) of splenic DLBCL were diagnosed as stage I compared to 28% (29,985/106,434) of all other types of DLBCL (p<0.01). Patients with stage I splenic DLBCL treated in the rituximab era had better OS than patients with stage I DLBCLs of other types treated during the same period [Figure 1; hazard ratio (HR)=0.62, 95% confidence interval (CI)=0.53-0.86; p<0.01].

The rate of splenectomy was lower after the approval of rituximab (82% vs. 72%, p=0.03). Splenectomy was associated with an improvement in DSS (HR=0.57, 95% CI=0.28-0.96; p=0.04). When analyzed by era, however, improved DSS with splenectomy was only seen in the pre-rituximab cohort (HR=0.51, 95% CI=0.17-1.08; p=0.04), but not in the rituximab-era cohort (Figure 2; HR=0.62, 95% CI=0.25-1.38; p=0.53). OS advantage with splenectomy was also seen only in the pre-rituximab era (HR=0.66, 95% CI=0.32-1.14; p=0.03) and not in the rituximab era (HR=0.74, 95% CI=0.37-1.43, p=0.45). Combining patients with and without splenectomy, there was a trend toward improved OS with the introduction of rituximab (Figure 3; HR=0.75, 95% CI=0.48-1.14; p=0.054). There was no significant difference in the utilization of radiation between these cohorts (6% pre-rituximab versus 3% rituximab era, p=0.13).

Our search of the Mitelman database found 1,413 patients with DLBCL, but none of them had stage I splenic DLBCL. We also identified 20 patients with non-Hodgkin lymphoma profiled by Caris Life Sciences, of whom only one had primary splenic DLBCL.

Discussion

Prior studies have shown that primary splenic lymphoma represents 1-6% of all non-Hodgkin's lymphomas (3, 4). Our study is mostly consistent with these findings as our SEER review found that 1% of stage I DLBCL was PSL, but primary splenic DLBCL was even less common in other databases. PSL is more likely to present as stage I disease compared to other types of DLBCLs and stage I splenic DLBCL appears to have a favorable prognosis relative to other stage I DLBCLs. It is more common in middle-aged patients, with a mean age of 66 years at diagnosis.

Current treatment of stage I primary splenic DLBCL often includes surgery and immunochemotherapy based on limited data (4). More robust data are available for the treatment of low-grade B-cell PSL, especially primary splenic marginal zone lymphoma (MZL). Early studies showed benefit of splenectomy as first-line therapy for splenic MZL (22). However, since the advent of rituximab, some have suggested that splenectomy can be abandoned as first-line treatment for splenic MZL as rituximab alone has 88-100% response rate (23, 24). Moreover, Musteata et al. suggested that early splenectomy along with combination chemotherapy was the optimal treatment for low-grade PSL, leading to higher response rates, progression-free survival, and OS compared to chemotherapy alone (25). For those unable to undergo splenectomy, local radiotherapy has historically been considered for low-grade PSL (25). Our review of splenic DLBCL found that radiation is rarely used and does not appear to influence outcomes.

One difficulty in assessing the best treatment for stage I splenic DLBCL is that most studies are retrospective and group all histological subtypes of PSL together. Small studies of PSL with DLBCL subtype show good response to splenectomy while most also received adjuvant chemotherapy/radiation (8). In a retrospective study of 87 patients with splenic DLBCL, splenectomy at diagnosis improved survival. The vast majority of these patients received adjuvant CHOP-based chemotherapy (92%), while 83% had treatment that included rituximab (26). In a small study of 59 patients with PSL (16 had intermediate- to high-grade lymphoma), the median survival was 108 months in those who underwent splenectomy and 24 months in those not treated surgically. However, rituximab was not available at the time of that study (4). With the advent of rituximab in 2006, the standard systemic treatment for DLBCL now includes this agent. It is reasonable to consider it also as standard treatment for splenic DLBCL. It is unclear if patients with surgically resected primary splenic DLBCL should undergo adjuvant treatment. Some studies have recommended splenectomy alone and very few have demonstrated the benefit of adjuvant chemotherapy following splenectomy in these patients (2-5, 24-26). However, since there is a paucity of data, we could rationally adopt the same strategy that is used for DLBCL patients with surgically resected localized extra nodal disease. This would include the use of CHOP plus rituximab for four cycles (5).

Figure 1.
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Figure 1.

Overall survival of patients with stage I splenic diffuse large B-cell lymphoma versus those with all other types of stage I diffuse large B-cell lymphomas assessed from time of diagnosis. Data source: Surveillance, Epidemiology, and End Results registry. CI: Confidence interval: HR: hazard ratio.

Our data show that there is a trend towards improved OS after the introduction of rituximab in patients with stage I splenic DLBCL. Prior studies of all stages of PSL in the pre-rituximab era suggested a 5-year survival rate of 31-40% (27). We found the median OS of patients with stage I splenic DLBCL in the post-rituximab era to be 11 years. We also showed that splenectomy improved DSS and OS in stage I splenic DLBCL, but the benefit was only seen prior to the introduction of rituximab. Therefore, it is still unclear if splenectomy is a necessary part of treatment in the era of rituximab. Splenectomy is irreversible and consequently leads to the loss of its multiple hematological and immunological functions. Our data show that splenectomy lost its impact on OS after introduction of rituximab. They also demonstrate that the usage of rituximab has reduced the rate of splenectomy without compromising OS. It is quite possible that chemotherapy alone can cure stage I splenic DLBCL like other early stage DLBCLs, but this has not yet been proven.

Figure 2.
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Figure 2.

Disease-specific survival of patients with stage I splenic diffuse large B-cell lymphoma treated with or without splenectomy during the rituximab era assessed from time of diagnosis. Data source: Surveillance, Epidemiology, and End Results registry.

Figure 3.
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Figure 3.

Overall survival of patients with stage I splenic diffuse large B-cell lymphoma in the pre-rituximab (PreR) era and rituximab era (R) assessed from time of diagnosis. Data source: Surveillance, Epidemiology, and End Results registry.

Historically splenectomy was considered the most effective therapy for PSL because it is both diagnostic and therapeutic (28, 29). Splenic biopsy or splenectomy is often required for definitive diagnosis of PSL (30). Moreover, of all patients assessed for splenomegaly, 16-57% have malignancy by tissue diagnosis, most commonly lymphoma (7, 16). However, the diagnosis of PSL may sometimes be achieved by examination, imaging, peripheral smear and bone marrow biopsy without the need for splenectomy. Ultrasound usually shows hypoechoic lesions, while computed tomography shows hypodense lesions (31, 32). More specifically for DLBCL of the spleen, imaging will show large nodular or small nodular pattern (33, 34). Moreover, 59-70% of patients with stage I splenic DLBCL have B-symptoms (26, 35). For splenic MZL, the bone marrow is invariably involved and the peripheral blood smear shows malignant cells in most PSL (22). However, the bone marrow is only involved in <10% of splenic DLBCL cases and the peripheral smear is often nondiagnostic (26). Iannitto and Tripodo reported that only 5% of all PSLs require splenectomy in addition to bone marrow biopsy and peripheral smear review for diagnosis, but it is unclear if this specifically applies to the DLBCL subtype (5). Therefore, splenectomy may still be required for the diagnosis of splenic DLBCL, but it is not clear that it is a therapeutic necessity.

Our SEER analysis found that the utilization of splenectomy for stage I splenic DLBCL has decreased with the introduction of rituximab without compromise of outcomes. Alternative databases added little to the understanding of the biology of stage I splenic DLBCL. Complications of splenectomy include infection and hemorrhage, which can be fatal at times. There has been an increased tendency in recent years towards splenic preservation to prevent these complications. We need more studies to demonstrate the clinical benefit of rituximab-based chemotherapy without splenectomy in stage I splenic DLBCL and the long-term survival outcomes.

  • Received August 23, 2017.
  • Revision received October 16, 2017.
  • Accepted October 18, 2017.
  • Copyright© 2017, International Institute of Anticancer Research (Dr. George J. Delinasios), All rights reserved

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Anticancer Research: 37 (12)
Anticancer Research
Vol. 37, Issue 12
December 2017
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Multi-Database Description of Primary Splenic Diffuse Large B-Cell Lymphoma
KENNETH P. BYRD, NAMRATHA R. VONTELA, BRENNAN MCCULLAR, MIKE G. MARTIN
Anticancer Research Dec 2017, 37 (12) 6839-6843;

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Multi-Database Description of Primary Splenic Diffuse Large B-Cell Lymphoma
KENNETH P. BYRD, NAMRATHA R. VONTELA, BRENNAN MCCULLAR, MIKE G. MARTIN
Anticancer Research Dec 2017, 37 (12) 6839-6843;
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Keywords

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