Hematopoietic stem cell transplantation in mantle cell lymphoma

A. K. Ganti1, P. J. Bierman1, J. C. Lynch2, R. G. Bociek1, J. M. Vose1 and J. O. Armitage1,*

1 Department of Internal Medicine, Division of Oncology/Hematology, and 2 Department of Preventive and Societal Medicine, University of Nebraska Medical Center, Omaha, NE, USA

* Correspondence to: Dr J. O. Armitage, Department of Internal Medicine, Division of Oncology-Hematology, 987680 Nebraska Medical Center, Omaha, NE 68198-7680, USA. Tel: +1-402-559-7290; Fax: +1-402-559-8597; Email: joarmita{at}unmc.edu


    Abstract
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Discussion
 References
 
Background: Patients with mantle cell lymphoma (MCL) have in general, lower response rates and overall survival (OS) than those with other B-cell non-Hodgkin's lymphomas. The role of hematopoietic stem cell transplantation (HSCT) in MCL is unclear. Hence we decided to study the clinical course of patients who received autologous and allogeneic HSCT for MCL.

Methods: Ninety-seven patients, (80 patients-autologous; 17 patients-allogeneic) who received a HSCT for mantle cell lymphoma were included in the study.

Results: The complete response rates at day 100 between the two groups were similar (73% vs. 62%). Day-100 mortality was higher in the allogeneic HSCT group (19% vs. 0%) (P < 0.01). The estimated 5-year relapse rates, 5-year event-free survival (EFS) and 5-year OS among the allogeneic HSCT patients were 21%, 44% and 49%, respectively, similar to 56%, 39% and 47% in the autologous group. Ten patients received HyperCVAD (hyperfractionated cyclophosphamide, vincristine, doxorubicin and dexamethasone + high-dose methotrexate and cytarabine) ± rituximab prior to transplant. There have been no relapses or deaths amongst these patients at a median follow-up of 16 months.

Conclusions: Patients treated with allogeneic HSCT had a lower relapse rate, but similar EFS and OS to autologous HSCT. Treatment of MCL with HyperCVAD ± rituximab followed by HSCT seems promising.

Key words: mantle cell lymphoma, autologous hematopoietic stem cell transplantation, allogeneic hematopoietic stem cell transplantation, HyperCVAD


    Introduction
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Discussion
 References
 
Mantle cell lymphoma (MCL) is a mature B-cell lymphoma with tumor cells that are typically CD5+ and CD23– and overexpress cyclin D1 [1Go]. MCL accounts for ~6% of adult non-Hodgkin's lymphomas [2Go]. In a Southwest Oncology Group (SWOG) study, Fisher et al. [3Go] reviewed 376 cases of disseminated low-grade lymphomas and found that MCL comprised ~10% of those cases. Patients with MCL are usually male (74%), present with advanced disease (71%) and have a median survival of 3–4 years [2Go, 4Go].

The response rates and overall survival in patients with MCL are poor. Fisher et al. [3Go], in their study of 36 patients with MCL, estimated an 8% 10-year failure-free survival, which was significantly lower than the other types of lymphomas. Multiple chemotherapeutic regimens have been used for MCL, including CHOP (cyclophosphamide, doxorubicin, vincristine and prednisone) [5Go], fludarabine [6Go], fludarabine and idarubicin [7Go], single-agent rituximab [8Go], CHOP + rituximab [9Go], VAD (vincristine, doxorubicin and dexamethasone) ± chlorambucil [10Go], and CHOP followed by DHAP (dexamethasone, cisplatin and cytarabine) [11Go], but none has shown clear superiority over the other with reported overall response rates (ORR) ranging from 30% to 90% and complete remission (CR) rates ranging from 10% to 90%. No regimen has consistently been proven to be curative and there were no major differences in the overall survival in many of these studies [5Go–12Go]. Recently, Romaguera et al. [13Go] presented their findings on 25 elderly patients who were treated with HyperCVAD (hyperfractionated cyclophosphamide, vincristine, doxorubicin and dexamethasone), alternating every 3 weeks with high doses of methotrexate and cytarabine. They had an ORR of 92%, CR rates of 68% and median failure-free survival of 15 months after 17 months of follow-up.

Two recent studies examined the role of immunotherapy in the treatment of MCL. The German Low Grade Lymphoma Study Group treated patients with relapsed MCL using rituximab, fludarabine, cyclophosphamide and mitoxantrone (R-FCM). They found that patients in the R-FCM arm had higher remission rates than FCM alone (62% versus 43%) [14Go]. Zelenetz et al. [15Go] enrolled patients with untreated MCL to sequential therapy with iodine I131 tositumomab (75 cGy) followed 13–16 weeks later by CHOP chemotherapy for six cycles. The ORR to induction with radioimmunotherapy was 83%: CR 50%; partial response (PR) 33%.

Since conventional chemotherapy does not offer cure in most patients with MCL, high-dose chemotherapy followed by hematopoietic stem cell transplant (HSCT) has been looked at in an effort to improve survival rates. Although high-dose chemotherapy followed by autologous HSCT improves overall survival, reports suggest that this approach might not cure this disease [16Go]. There are a number of reports that have shown prolonged CRs with allogeneic HSCT even in cases of relapse after autologous HSCT [17Go–19Go].

In the absence of randomized clinical trials, the exact role of HSCT in the treatment of MCL remains unclear. Also it is not known which type of transplantation represents the better therapy for patients with MCL. Hence we decided to study the clinical course of the disease in patients who received autologous and allogeneic HSCT for MCL, to determine whether the transplant modality had any effect on the clinical outcome of the patients.


    Patients and methods
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Discussion
 References
 
Ninety-six patients who received HSCT for MCL at the University of Nebraska Medical Center between December 1988 and March 2003 were included in the study. These included 80 patients who received an autologous transplant and 17 patients who received a myeloablative allogeneic transplant from a matched sibling donor. One patient received an autologous transplantation initially, and then went on to receive a full intensity allogeneic transplantation following relapse. Data collected included: age at transplant, sex of the patient, race/ethnicity, time from diagnosis to transplant, number of prior chemotherapeutic regimens, stage of the disease at transplant, extranodal involvement, bone marrow involvement, lactate dehydrogenase level, disease status at transplant, chemosensitivity of the tumor, the conditioning regimen and the rescue product.

Primary end points considered were response at day 100, mortality at day 100, relapse rate, event-free survival (EFS) and overall survival (OS). Response at day 100 was classified into CR, PR and no response or progressive disease. Disease-free survival (DFS) was defined as survival without evidence of worsening disease. For analyses of DFS, relapses or deaths from any cause were considered as events. For analyses of overall survival, events were deaths from any cause.

We were also interested in estimating the impact of prior therapy with HyperCVAD and high dose methotrexate and cytarabine ± rituximab on outcomes following transplantation. Hence we performed a subgroup analysis of patients who were transplanted after 2000 in order to use non-HyperCVAD cases from a comparable time period. This time frame was chosen in order to ensure that the two groups were comparable in all aspects except therapy with HyperCVAD.

The Wilcoxon rank-sum test and {chi}2-test were used as appropriate to compare patient, disease and transplant characteristics between autologous and allogeneic transplant recipients. The cumulative incidence estimator was used to estimate the relapse rate and the Kaplan–Meier method was used to estimate the EFS and OS distribution. The log-rank test was to compare time-to-event variables.


    Results
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Discussion
 References
 
Patient characteristics
We analyzed 96 patients who received HSCT for MCL. Eighty patients received an autologous transplantation, while 17 patients received an allogeneic transplantation. The patient who received both autologous and allogeneic HSCT was included in both categories for descriptive purposes, but for comparison between autologous and allogeneic transplants, only the first transplant was included (i.e. the patient was included in the autologous transplant group). The patient, disease and transplant characteristics are detailed in Table 1.


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Table 1. Patient disease and transplant characteristics

 
Patients who received an autologous transplant were more likely to be older (56 versus 47 years) (P <0.01) and were less likely to receive a conditioning regimen containing total body irradiation (9% versus 94%) (P <0.0001) than patients who received an allogeneic transplant. There were no other statistically significant differences in the distribution of patient, disease and transplant characteristics between the patients receiving autologous and allogeneic transplants.

Outcomes
The median follow-up of surviving patients is 33 months (range 3–121). There was no statistically significant difference in the CR rate between patients receiving autologous and allogeneic transplants (73% versus 62%) (Table 2). Three deaths occurred in the first 100 days after transplant among recipients of allogeneic transplants (19%) compared with no deaths among those receiving autologous transplants (P <0.01). The causes of death among these patients were: acute respiratory distress syndrome, septic shock and Aspergillus infection. The estimated 5-year relapse rate was 21% among patients receiving an allogeneic transplant compared with 56% for those receiving an autologous transplant (P=0.11) (Figure 1). The estimated 5-year EFS was 44% for allogeneic transplants and 39% for autologous transplants (P=0.85) (Figure 2). The estimated 5-year OS was 49% for allogeneic transplants and 47% for autologous transplants (P=0.51) (Figure 3).


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Table 2. Response at day 100 in patients receiving autologous and allogeneic transplantation

 


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Figure 1. Estimated relapse rate among patients with autologous and allogeneic transplantation.

 


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Figure 2. Estimated event-free survival among patients with autologous and allogeneic transplantation.

 


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Figure 3. Estimated overall survival among patients with autologous and allogeneic transplantation.

 
We performed a subgroup analysis of 33 patients who received their transplantation after 2000. Of these, 10 patients (eight autologous HSCT, two allogeneic HSCT) received chemotherapy with HyperCVAD ± rituximab, while 23 patients (19 autologous HSCT, four allogeneic HSCT) did not receive HyperCVAD. There were no differences amongst the characteristics of patients who did and did not receive HyperCVAD (Table 3).


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Table 3. Patient disease and transplant characteristics of patients transplanted after 2000

 
After a median follow-up of 16 months (range 3–30), seven out of 23 patients (30%) who did not receive HyperCVAD had a relapse, compared with none of 10 patients (0%) who were treated with HyperCVAD (P=0.07) (Figure 4). In addition, there were no deaths in the HyperCVAD group, compared with four deaths (17%) among patients who did not receive HyperCVAD (P=0.21) (Figure 5). Also, there was no effect of prior therapy with HyperCVAD on the EFS amongst the 25 patients who received an autologous transplant after 2000 (P=0.14) (Figure 6).



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Figure 4. Relapse rate in patients based on prior chemotherapy with HyperCVAD (hyperfractionated cyclophosphamide, vincristine, doxorubicin and dexamethasone).

 


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Figure 5. Overall survival in patients based on prior chemotherapy with HyperCVAD (hyperfractionated cyclophosphamide, vincristine, doxorubicin and dexamethasone).

 


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Figure 6. Relapse rate in patients with autologous transplant based on prior chemotherapy with HyperCVAD (hyperfractionated cyclophosphamide, vincristine, doxorubicin and dexamethasone).

 

    Discussion
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Discussion
 References
 
HSCT has been used in order to improve the poor prognosis in MCL, but its role has not yet been clearly established and the patients most likely to benefit from it have not been clearly identified. A recent study by the European Blood and Bone Marrow Transplant and Autologous Blood and Marrow Transplant registries evaluated 195 patients following autologous HSCT and found that the 2- and 5-year OS were 76% and 50%, and progression-free survival were 55% and 33%, respectively. The study concluded that autologous HSCT improved survival in MCL [20Go]. In a study performed at the M. D. Anderson Cancer Center, 16 patients with MCL received allogeneic HSCT. OS and failure-from-progression (FFP) at 3 years were both 55%. Patients with chemosensitive disease had a better FFP and OS at 1 year than those who were refractory to conventional chemotherapy (90% versus 44%) [17Go].

Our present study compared autologous and allogeneic HSCT for the treatment of MCL. We performed a univariate analysis to compare the two groups, and evaluate if the differences seen could be attributed to differences in patient or disease characteristics. We found that CR rate at day 100, 5-year estimated OS and 5-year estimated EFS were not significantly different amongst patients receiving autologous and allogeneic HSCT (73%, 47% and 39% versus 62%, 49% and 44%, respectively). These findings are similar to those seen in similar studies of other hematological malignancies like multiple myeloma, Hodgkin's disease and acute myeloid leukemia [21Go–23Go].

The estimated 5-year relapse rate was 21% among patients receiving an allogeneic transplant, compared with 56% for those receiving an autologous transplant (P=0.11). We feel that our study may have been underpowered to detect a difference between the two groups. In a similar study comparing autologous and allogeneic transplantation in patients with lymphoblastic lymphoma, Levine et al. [24Go] found that among patients who survived in remission for 6 months following HSCT, patients with autologous HSCT were more likely to suffer a subsequent relapse than patients who received allogeneic transplants, leading to a statistically significant difference in the cumulative incidence of relapse by 1 year after transplantation. The reasons for the lower risk of relapse are unclear but may involve a graft-versus-lymphoma effect. This could be similar to the graft-versus-leukemia effect that has clearly been demonstrated [25Go, 26Go]. Another possible explanation of the lower incidence of relapse is that re-infusion of autologous stem cells contaminated with tumor cells contributed to the higher relapse rate in the autologous HSCT group. This was borne out in a recent study in which patients who received unpurged autografts had a two-fold greater relapse risk than the recipients of purged autografts [27Go].

Patients receiving allogeneic HSCT had a significantly higher early mortality compared with patients receiving autologous HSCT (19% versus 0%; P <0.01). The reported causes of death were acute respiratory distress syndrome, septic shock and Aspergillus infection. One of the reasons for this increased mortality may be that the receipients of allogeneic HSCT were more likely to receive radiation-containing conditioning regimens (94% versus 9%). It is possible that this contributed to increased organ toxicity and/or slower engraftment, leading to an overall increase in immediate transplant-related mortality. A similar phenomenon of increased transplant-related mortality has been reported in other studies comparing autologous and allogeneic transplantations for other hematological malignancies as well [21Go–23Go]. Khouri et al. [28Go] performed a study on 18 patients in order to determine the efficacy of non-ablative allogeneic stem-cell transplantation in patients with relapsed MCL. They found a complete donor cell engraftment and no evidence of acute graft-versus-host disease or transplant-related deaths at 100 days. In their study, 17 out of the 18 patients achieved CR. This suggests that, selection bias notwithstanding, non-ablative allogeneic transplantation is a potentially effective strategy for patients with MCL.

An interesting and potentially important finding in our study was the absence of relapses or other adverse events amongst patients receiving HSCT after chemotherapy with HyperCVAD. Although the number of patients in our series was small and the follow-up short, our results confirm the findings of Khouri et al. [29Go], who treated 33 patients with aggressive MCL with HyperCVAD alternating with high-dose methotrexate and cytarabine for four cycles and then consolidated them with HSCT. They achieved a CR in all patients undergoing a transplant. At a median follow-up of 49 months, their estimated 5-year OS and DFS were 77% and 43%, respectively.

Our findings, like those from previous similar studies, suggest that the choice between allogeneic versus autologous stem cells does not affect the overall transplantation outcome. However, we did find almost 40% 5-year estimated EFS (44% and 39% for allogeneic and autologous transplants, respectively) and almost 50% 5-year estimated OS (49% and 47% for allogeneic and autologous transplants, respectively) in patients with MCL, regardless of the type of transplant. The pattern of treatment failure between autologous and allogeneic HSCT differs and may help in the design of future strategies. Because most patients lack an available allogeneic donor, new strategies to improve the outcome of autologous transplantation are needed. The lack of an obvious plateau in relapses after autologous transplantation indicates that late disease control is a major problem. Incorporation of current or future monoclonal antibody therapies, perhaps as post-transplantation consolidation, may be of value for these patients. Whichever source of hematopoietic stem cells is selected, greater cytoreduction before the transplant with an effective regimen such as HyperCVAD + rituximab may optimize results.


    Acknowledgements
 
This work was presented at the annual meeting of the American Society of Blood and Marrow Transplantation, Orlando, FL, 2004, and the abstract was published in the meeting proceedings. There was no external source of funding for this work.

Received for publication November 4, 2004. Accepted for publication November 9, 2004.


    References
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Discussion
 References
 
1. Barista I, Romaguera JE, Cabanillas F. Mantle-cell lymphoma. Lancet Oncol 2001; ii: 141–148.

2. Armitage JO, Weisenberger DD. New approach to classifying non-Hodgkin's lymphomas: clinical features of the major histologic subtypes. Non-Hodgkin's Lymphoma Classification Project. J Clin Oncol 1998; 16: 2780–2795.[Abstract]

3. Fisher RI, Dahlberg S, Nathwani BN et al. A clinical analysis of two indolent lymphoma entities: mantle cell lymphoma and marginal zone lymphoma (including the mucosa-associated lymphoid tissue and monocytoid B-cell subcategories): a Southwest Oncology Group study. Blood 1995; 85: 1075–1082.[Abstract/Free Full Text]

4. Bosch F, Lopez-Guillermo A, Campo E et al. Mantle cell lymphoma: presenting features, response to therapy, and prognostic factors. Cancer 1998; 82: 567–575.[CrossRef][ISI][Medline]

5. Meusers P, Engelhard M, Bartels H et al. Multicentre randomized therapeutic trial for advanced centrocytic lymphoma: anthracycline does not improve the prognosis. Hematol Oncol 1989; 7: 365–380.[ISI][Medline]

6. Foran JM, Rohatiner AZ, Coiffier B et al. Multicenter phase II study of fludarabine phosphate for patients with newly diagnosed lymphoplasmacytoid lymphoma, Waldenstrom's macroglobulinemia, and mantle-cell lymphoma. J Clin Oncol 1999; 17: 546–553.[Abstract/Free Full Text]

7. Zinzani PL, Magagnoli M, Moretti L et al. Randomized trial of fludarabine versus fludarabine and idarubicin as frontline treatment in patients with indolent or mantle-cell lymphoma. J Clin Oncol 2000; 18: 773.[Abstract/Free Full Text]

8. Foran JM, Rohatiner AZ, Cunningham D et al. European phase II study of rituximab (chimeric anti-CD20 monoclonal antibody) for patients with newly diagnosed mantle-cell lymphoma and previously treated mantle-cell lymphoma, immunocytoma, and small B-cell lymphocytic lymphoma. J Clin Oncol 2000; 18: 317–324.[Abstract/Free Full Text]

9. Howard OM, Gribben JG, Neuberg DS et al. Rituximab and CHOP induction therapy for newly diagnosed mantle-cell lymphoma: molecular complete responses are not predictive of progression-free survival. J Clin Oncol 2002; 20: 1288–1294.[Abstract/Free Full Text]

10. Gressin R, Legouffe E, Leroux D et al. Treatment of mantle-cell lymphomas with the VAD +/– chlorambucil regimen with or without subsequent high-dose therapy and peripheral blood stem-cell transplantation. Ann Oncol 1997; 8 (Suppl 1): 103–106.[CrossRef][Medline]

11. Lefrere F, Delmer A, Suzan F et al. Sequential chemotherapy by CHOP and DHAP regimens followed by high-dose therapy with stem cell transplantation induces a high rate of complete response and improves event-free survival in mantle cell lymphoma: a prospective study. Leukemia 2002; 16: 587–593.[CrossRef][ISI][Medline]

12. Teodorovic I, Pittaluga S, Kluin-Nelemans JC et al. Efficacy of four different regimens in 64 mantle-cell lymphoma cases: clinicopathologic comparison with 498 other non-Hodgkin's lymphoma subtypes. European Organization for the Research and Treatment of Cancer Lymphoma Cooperative Group. J Clin Oncol 1995; 13: 2819–2826.[Abstract]

13. Romaguera JE, Khouri IF, Kantarjian HM et al. Untreated aggressive mantle cell lymphoma: results with intensive chemotherapy without stem cell transplant in elderly patients. Leuk Lymphoma 2000; 39: 77–85.[ISI][Medline]

14. Dreyling MH, Forstpointner R, Repp R et al. Combined immuno-chemotherapy (R-FCM) results in superior remission and survival rates in recurrent follicular and mantle cell lymphoma–Final results of a prospective randomized trial of the German Low Grade Lymphoma Study Group (GLSG). Blood 2003; 102: 103a.

15. Zelenetz AD, Donnelly G, Halaas J et al. Initial treatment of mantle cell lymphoma with sequential radioimmunotherapy with tositumoamb/iodine I131 I-tositumoamb followed by CHOP chemotherapy results in a high complete remission rate. Blood 2003; 102: 406a.

16. Jindra P, Koza V, Svojgrova M et al. Frontline transplantation of autologous CD34+ selected blood cells for advanced mantle cell lymphoma: no evidence of long-term cure: a single centre experience. Bone Marrow Transplant 2000; 26: 1138–1139.[CrossRef][ISI][Medline]

17. Khouri IF, Lee MS, Romaguera J et al. Allogeneic hematopoietic transplantation for mantle-cell lymphoma: molecular remissions and evidence of graft-versus-malignancy. Ann Oncol 1999; 10: 1293–1299.[Abstract]

18. Kröger N, Hoffknecht M, Kruger W et al. Allogeneic bone marrow transplantation for refractory mantle cell lymphoma. Ann Hematol 2000; 79: 578–580.[CrossRef][ISI][Medline]

19. Martinez C, Carreras E, Rovira M et al. Patients with mantle-cell lymphoma relapsing after autologous stem cell transplantation may be rescued by allogeneic transplantation. Bone Marrow Transplant 2000; 26: 677–679.[CrossRef][ISI][Medline]

20. Vandenberghe E, Ruiz de Elvira C, Loberiza FR et al. Outcome of autologous transplantation for mantle cell lymphoma: a study by the European Blood and Bone Marrow Transplant and Autologous Blood and Marrow Transplant Registries. Br J Haematol 2003; 120: 793–800.[CrossRef][ISI][Medline]

21. Varterasian M, Janakiraman N, Karanes C et al. Transplantation in patients with multiple myeloma: a multicenter comparative analysis of peripheral blood stem cell and allogeneic transplant. Am J Clin Oncol 1997; 20: 462–466.[CrossRef][ISI][Medline]

22. Milpied N, Fielding AK, Pearce RM et al. Allogeneic bone marrow transplant is not better than autologous transplant for patients with relapsed Hodgkin's disease. European Group for Blood and Bone Marrow Transplantation. J Clin Oncol 1996; 14: 1291–1296.[Abstract]

23. Cassileth PA, Harrington DP, Appelbaum FR et al. Chemotherapy compared with autologous or allogeneic bone marrow transplantation in the management of acute myeloid leukemia in first remission. N Engl J Med 1998; 339: 1649–1656.[Abstract/Free Full Text]

24. Levine JE, Harris RE, Loberiza FR Jr et al. A comparison of allogeneic and autologous bone marrow transplantation for lymphoblastic lymphoma. Blood 2003; 101: 2476–2482.[Abstract/Free Full Text]

25. Van Besien KW, de Lima M, Giralt SA et al. Management of lymphoma recurrence after allogeneic transplantation: the relevance of graft-versus-lymphoma effect. Bone Marrow Transplant 1997; 19: 977–982.[CrossRef][ISI][Medline]

26. Sykes M, Preffer F, McAfee S et al. Mixed lymphohaemopoietic chimerism and graft-versus-lymphoma effects after non-myeloablative therapy and HLA-mismatched bone-marrow transplantation. Lancet 1999; 353: 1755–1759.[CrossRef][ISI][Medline]

27. Bierman PJ, Sweetenham JW, Loberiza FR Jr et al. Syngeneic hematopoietic stem-cell transplantation for non-Hodgkin's lymphoma: a comparison with allogeneic and autologous transplantation. The Lymphoma Working Committee of the International Bone Marrow Transplant Registry and the European Group for Blood and Marrow Transplantation. J Clin Oncol 2003; 21: 3744–3753.[Abstract/Free Full Text]

28. Khouri IF, Lee MS, Saliba RM et al. Nonablative allogeneic stem-cell transplantation for advanced/recurrent mantle-cell lymphoma. J Clin Oncol 2003; 21: 4407–4412.[Abstract/Free Full Text]

29. Khouri IF, Saliba RM, Okoroji GJ et al. Long-term follow-up of autologous stem cell transplantation in patients with diffuse mantle cell lymphoma in first disease remission: the prognostic value of beta2-microglobulin and the tumor score. Cancer 2003; 98: 2630–2635.[CrossRef][ISI][Medline]





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