Myelofibrosis Stem cell transplantation for myelofibrosis: a report from two Canadian centers
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1 (23) 32, 35 4 & 23 Nature Publishing Group All rights reserved /3 $25. Myelofibrosis Stem cell transplantation for myelofibrosis: a report from two Canadian centers A Daly 1, K Song 2, T Nevill 2, S Nantel 2, C Toze 2, D Hogge 2, D Forrest 2, J Lavoie 2, H Sutherland 2, J Shepherd 2, WHasegawa 1, J Lipton 1, H Messner 1 and T Kiss 1 1 Allogeneic Bone Marrow Transplant Program, Princess Margaret Hospital, University Health Network, Toronto, Ont., Canada; and 2 Leukemia/BMT Program of British Columbia, Vancouver General Hospital, British Columbia Cancer Agency, Vancouver, British Columbia, Canada Summary: We describe the course of 25 patients with myelofibrosis (MF) due to agnogenic myeloid metaplasia (n ¼ 19) or essential thrombocytosis (n ¼ 6) who underwent allogeneic stem cell transplantation (SCT) at one of two Canadian centers. The median age at transplantation was 48.7 (IQR ) years and transplantation was carried out at a median of 1.7 (IQR ) months after diagnosis. Granulocyte engraftment (absolute neutrophil count /l) occurred at a median of 2 days after transplantation for splenectomized patients, compared with 27.5 days for nonsplenectomized individuals (P ¼.3). Increased risk of grade II IV acute graft-versus-host disease (P ¼.4) was noted in patients transplanted after splenectomy. Patients with MF received U of packed red blood cells per day over the first 18 days after transplantation, and remained dependent on red blood cell transfusions for a median of 123 (IQR 48 25) days. Complete remission of MF was documented in 33% of evaluable patients. The 1year cumulative nonrelapse mortality was 48.3%. Median survival for this group of patients was 393 (IQR ) days, with a projected 2-year overall survival of 41%. We conclude that allogeneic SCT offers a reasonable chance for prolonged survival in patients with advanced MF, but this occurs at the cost of considerable toxicity and nonrelapse mortality. (23) 32, doi:1.138/sj.bmt Keywords: stem cell transplant; allogeneic; myelofibrosis; agnogenic myeloid metaplasia; essential thrombocytosis; graft-versus-host disease; transfusion requirements Agnogenic myeloid metaplasia (AMM) and essential thrombocytosis (ET) are chronic myeloproliferative disorders that result in fibrosis of the bone marrow microenvironment and displacement of hematopoiesis to Correspondence: Dr A Daly, Department of Medical Oncology and Hematology, Princess Margaret Hospital, 61 University Ave, Toronto, Ont., Canada M5G 2M9 Received 16 January 23; accepted 3 February 23 extramedullary sites. Both of these disorders may progress to bone marrow failure or acute leukemia, although patients with ET may do so more slowly than those with AMM. Once significant myelofibrosis (MF) has occurred patients may develop portal hypertension related to massive splenomegaly and succumb to infection or hemorrhage. There is no conventional curative therapy for MF, standard treatment is supportive and the goals of therapy include correction of cytopenias with transfusion of blood products and use of low-dose chemotherapy or interferon to control systemic symptoms. 1 Patients may require splenectomy because of splenic pain or mass effect, although patients with MF have increased morbidity and mortality with this procedure. 2 AMM carries the worst prognosis of any of the chronic myeloproliferative disorders, and MF is generally a late event in the course of ET. 3 Allogeneic stem cell transplantation (SCT) is an accepted form of treatment for patients with hematopoietic stem cell disorders, 4 and offers the potential for long-term resolution of MF. 5 Several case reports have documented reversal of MF 6 8 and normalization of ferrokinetic studies 9 following allogeneic SCT for this disorder. Despite these results, significant concerns have been raised regarding engraftment of allogeneic blood stem cells within a fibrotic bone marrow microenvironment. 1 More recently, it was found that engraftment times were no different in patients with and without MF. 11 In this report we describe the experience of two Canadian centers with allogeneic SCT for the treatment MF in patients with AMM or ET. Patients and methods Patients Between August 199 and June 22, 25 adult patients with MF underwent allogeneic SCT at Princess Margaret Hospital, Toronto, Ontario and Vancouver General Hospital, Vancouver, British Columbia. Diagnoses of AMM satisfied the criteria of the Italian Consensus Conference, 12 while diagnoses of ET were based on the criteria of the Polycythemia Vera Study Group. 13 None of the patients in this study had received intensive chemotherapy for acute leukemia prior to undergoing
2 36 SCT. Treatment with low-dose chemotherapy, interferon and splenectomy was at the discretion of the treating physician. Patients with ET were considered for transplantation after becoming dependent on transfusions or once systemic symptoms developed. Pretransplant characteristics are summarized in Table 1. Nine patients had systemic symptoms and 19 patients had elevated serum lactate dehydrogenase at the time of transplantation. Bone marrow karyotype Cytogenetic testing was carried out on 19 patients on 23 separate occasions. Cytogenetic abnormalities were present in seven patients at diagnosis (Table 2). Samples failed to produce dividing cells for analysis in six cases and in six cases no abnormalities were detected. Clonal evolution occurred on four occasions, three times in patients with prior cytogenetic abnormalities and once in a patient with a previously normal karyotype. Transplant methods The preparative regimen consisted of cyclophosphamide and total body irradiation (n ¼ 23) or oral busulfan and cyclophosphamide (n ¼ 2). 14,15 All patients received standard cyclosporine A and short-course methotrexate for acute graft-versus-host disease (GVHD) prophylaxis. 16 Stem cell source and histocompatibility results are given in Table 3. Recipients of bone marrow from related donors Table 1 SCT Pretransplant characteristics of MF patients undergoing Characteristic Value Total N=25 Median age (IQR), years 48.7 (45.9.4) Male/female 18/7 Time from diagnosis of MF (IQR), months 1.7 ( ) Post-ET 6 Post-AMM 19 Lille risk score Low 3 Intermediate 9 High 7 Prior therapy Low-dose chemotherapy 8 Interferon 1 Splenectomy 7 Note: IQR=interquartile range; MF=myelofibrosis; ET=essential thrombocytosis; AMM=agnogenic myeloid metaplasia. Table 2 Results of G-banding cytogenetic testing of MF patients undergoing allogeneic SCT Result Samples (n=23) Normal 6 Failed to divide 6 Del (2) (q11) 2 Inv (12) (q15) 2 +8 or Complex 1 Clonal evolution (on retesting) 4 received a median of 2.77 (IQR ) 1 8 MNC/kg, while patients transplanted from matched unrelated bone marrow donors were given a median of 3.7 (IQR.88 4.) 1 8 MNC/kg. Two patients given G-CSF mobilized peripheral blood received and CD34 + cells/kg. Bone marrow was red blood cell depleted in the case of major ABO blood group incompatibility (n ¼ 7). Patients were given transfusions of packed red blood cells if hemoglobin fell to less than 8 g/l or at a higher level if clinically indicated. Prophylactic platelet transfusions were given to patients with platelet counts of less than /l or at higher levels if patients were considered to be at high risk of bleeding. One unit of single donor apheresis platelets or five units of random donor platelets were given, depending upon the availability of the single donor products on the day of transfusion. Recipients in whom either member of the donor recipient pair was positive for anti-cytomegalovirus antibodies prior to transplantation underwent routine screening and pre-emptive therapy with ganciclovir. Statistics Outcomes were defined according to standard criteria. Granulocyte engraftment was taken as the first of 2 days of an absolute granulocyte count /l. Platelet engraftment was defined as the first day on which the platelet count exceeded /l unsupported by transfusion. GVHD was diagnosed clinically and graded according to established criteria. 17,18 Hepatic veno-occlusive disease (VOD) was diagnosed according to the criteria of MacDonald et al 19 and graded according to the National Cancer Institute Common Toxicity Criteria. 2 The Lille score, applied retrospectively to blood counts obtained at the time of diagnosis of AMM, was used to determine each patient s risk category as described. 21 Criteria for response and progressive disease were defined prospectively as follows: complete remission (CR) was defined as the presence of normal blood counts, absence of splenomegaly on physical examination and absence of bone marrow fibrosis on bone marrow trephine biopsy. Complete Table 3 Transplant-related variables for 25 patients undergoing allogeneic Characteristic Number Conditioning regimen Cyclophosphamide and TBI 23 Busulfan and cyclophosphamide 2 GVHD prophylaxis Cyclosporine and methotrexate 25 Stem cell source Bone marrow 22 G-CSF mobilized blood 2 G-CSF stimulated bone marrow 1 Bone marrow donor type Matched related donor 13 Mismatched related donor 2 Matched unrelated donor 1 Major blood group incompatibility 7 Note: TBI=total body irradiation; G-CSF=granulocyte colony stimulating factor.
3 remission with low platelets (CRP) was defined as for CR with the exception of a platelet count below the normal range, while remaining platelet transfusion independent. Progressive disease was defined as ongoing or recurrent evidence of a myeloproliferative disease or transformation to acute leukemia. Summary statistics such as median and interquartile range are reported in order to describe the cohort, and outcomes for which there was variable or incomplete follow-up were described according to the method of Kaplan and Meier. 22 Categorical variables were compared using Fisher s exact test, while Student s t-test was used to compare means of continuous variables. Results Engraftment A total of 22 patients survived for more than 3 days and were therefore evaluable for engraftment. Of these, 2 patients achieved a neutrophil count greater than / l a median of 25 days after transplantation. Two patients (9.1%) experienced primary engraftment failure but engrafted after a second transplant from the same donor. In total, 17 patients achieved a platelet count of greater than /l, at a median of 35 days post-transplant. In all, 11 patients achieved a platelet count greater than 1 9 /l at a median of 27 days after transplantation. Neutrophil engraftment, but not platelet engraftment, was significantly affected by pretransplant splenectomy. The time to neutrophil recovery was shorter in patients who underwent transplant at any time following a splenectomy (2 days vs 27.5 days, P ¼.3) (Figure 1a). Prior splenectomy did not affect the time to platelet recovery (Figure 1b). Transplantation of stem cells from related or unrelated donors did not affect engraftment of neutrophils (P ¼.75) or platelets (P ¼.27). The impact of age at transplantation, etiology of MF, Lille score at diagnosis, presence of cytogenetic abnormalities, elevated lactate dehydrogenase, systemic symptoms and time from diagnosis of MF to SCT on neutrophil engraftment is shown in Table 4. None of these factors influenced engraftment. All patients required transfusion of blood products after transplantation. Detailed transfusion data were available for patients transplanted at Princes Margaret Hospital (n ¼ 17). Patients received a median of 18.5 (IQR ) U of packed red blood cells and 12 (IQR ) U of apheresis platelets after transplantation. The median number of random donor platelets was 5 (IQR 25.5). The median time to transfusion independence for red blood cells was 123 days. Patients transplanted at Princess Margaret Hospital were given an average of U of packed red blood cells per day over the first 18 days after transplantation. Toxicity Hepatic VOD was diagnosed in 9/25 patients. Six patients had grade 1 2 VOD, while two patients had grade 3 and one patient had grade 4. Acute GVHD (grade II IV) occurred in 13 patients, 5/15 related donor and 8/1 unrelated donor SCT recipients. Grade III IV acute GVHD occurred in four recipients of transplants, all following unrelated donor SCT. In total, 17 patients survived for more than days after transplant and were evaluable for chronic GVHD. Of these, 1 patients developed chronic GVHD, which was limited in four patients and extensive in six patients. Splenectomy was associated with an increased risk of grade II IV (P ¼.4) but not grade III IV (P ¼ NS) acute GVHD or chronic GVHD (P ¼ NS). Five patients (2%) died of transplant-related causes in the first days after SCT. The cumulative risk of transplant-related mortality over the course of the first year after SCT was 48.3%. Response to treatment Bone marrow biopsies were carried out on 18 patients following SCT. Only patients with repeat biopsies were evaluable for response according to the response criteria we 37 a Neutrophil engraftment b Platelet engraftment Percent engrafted Splenectomy No Splenectomy P =.3 Percent engrafted Splenectomy No Splenectomy P = Time 1 2 Engraftment Figure 1 Time to recovery of (a) neutrophil (ANC4.5) and (b) platelet (platelets42) counts following SCT for myelofibrosis.
4 38 Table 4 Impact of selected disease-associated and prognostic variables on outcome of stem cell transplantation for MF Variable Time to ANC>.5 (Days) P Time to minimal or no fibrosis (Days) P 2-year survival (%) Age at SCT o48.7 years X48.7 years Etiology of MF ET AMM Lille Score (AMM only) or Cytogenetics Abnormal Other Lactate dehydrogenase o2 Normal X2 Normal Systemic Symptoms Absent Present Time from MF to SCT o1.7 months X1.7 months Note: ANC=absolute neutrophil counts; SCT=stem cell transplant; MF=myelofibrosis; ET=essential thrombocytosis; AMM=agnogenic myeloid metaplasia; Other cytogenetics=normal, failed to divide or not tested. P selected. A total of 1 cases (56%) were reported as showing minimal or no fibrosis a median of 363 days after transplantation. The impact of selected disease-associated and prognostic variables on resolution of fibrosis is shown in Table 4. None of the variables analyzed influenced the time to achieve minimal or no fibrosis. Seven of nine (78%) patients surviving for more than 1 year from the time of transplantation were free of fibrosis at the time of the last biopsy. Only three of nine (33%) patients who survived for less than 1 year showed minimal or no fibrosis on the last biopsy. CR was documented in six of 18 (33%) patients with repeat biopsies, and CRP was confirmed in two patients (11%). Both patients with CRP were receiving treatment for GVHD at the time of their most recent evaluation Three patients underwent transformation to acute leukemia days after transplantation and died having received supportive care alone days after their transplants. A fourth patient had persistent splenomegaly following his bone marrow transplant. Spleen size increased starting 794 days after transplantation and the patient was lost to follow-up 2695 days after transplantation, at which point he was receiving low-dose chemotherapy for splenic pain. A bone marrow biopsy at the time of increasing splenomegaly demonstrated megakaryocytic hyperplasia with no increase in blast cells. Survival In total, 11 patients remain alive months following transplantation (median 35 months). Nine have had follow-up bone marrow biopsies, with eight showing minimal or no fibrosis. Five surviving patients meet our criteria for CR, with two further patients showing a qualified remission with a low platelet count. The median survival for patients in this cohort was 393 days and median progression-free survival was 287 days. Survival was not influenced by pretransplant splenectomy (P ¼.95) or transplantation from an unrelated donor (P ¼.16). The impact of age at SCT, etiology of MF, Lille score at diagnosis, presence of cytogenetic abnormalities, elevated lactate dehydrogenase, systemic symptoms and time from diagnosis to SCT is shown in Table 4. None of these variables influenced 2-year survival. The causes of death were progressive disease (n ¼ 3), GVHD (n ¼ 3), respiratory failure (n ¼ 3), VOD (n ¼ 2), multiorgan failure (n ¼ 2) and bowel perforation (n ¼ 1). Cases of respiratory failure were caused by Cytomegalovirus pneumonia, Pneumocystis pneumonia or diffuse alveolar hemorrhage in one case each. The actuarial 2-year survival was 41% (41.7% in ET, 41.4% in AMM; P ¼.97), while progression-free survival at 2 years was 37.4% (41.7% in ET, 36.8% in AMM; P ¼.86) (Figure 2). Discussion Current supportive care strategies for patients with MF have not increased survival significantly beyond the 3 5 years expected for patients with this condition. In the present study we have shown that allogeneic SCT leads to long-term disease control in some patients, although the observed treatment-related toxicity was significant. Our criteria for complete remission in MF include reversal of fibrosis and splenomegaly and normalization of blood counts. Guardiarola et al 23 have used the term histohematological remission for the same triad of findings. The labile nature of blood counts in the post-transplant period led to the establishment of a more qualified CR, a CR with isolated low platelet counts. Using these criteria we have demonstrated the occurrence of complete remissions in six of 18 evaluable patients, while a further two
5 a Actuarial survival b Progression-free survival 39 Percent survival Progression-free Survival (days) Survival (days) Figure 2 Product limit estimates of (a) overall survival and (b) progression-free survival for recipients of allogeneic bone marrow transplants for MF because of agnogenic myeloid metaplasia and essential thrombocytosis. patients had CRP. In their study, Guardiarola et al 23 found a similar response rate and reported that such remissions were achieved in 22 out of 55 patients transplanted. None of the eight patients whom we report who achieved a CR has relapsed after a median of 35 months, suggesting that reversal of fibrosis and resumption of normal hematopoiesis may be sufficient for long-term survival in this disease. The role of splenectomy in MF remains controversial. Splenectomy is generally reserved for patients with splenic pain or local compressive symptoms, or for patients in whom splenic sequestration is responsible for cytopenias. We have shown that neutrophil recovery occurred a median of 7 days earlier in patients who had undergone splenectomy at any time prior to transplantation, although splenectomy did not lead to improved survival in these patients. We were unable to demonstrate an effect of splenectomy on platelet recovery, although such a relation has been suggested previously. 23 Although splenectomy may be associated with beneficial effects on recovery of blood counts, it cannot be universally recommended. Recent reports suggest that the mortality rate for patients with MF undergoing splenectomy ranges between 13 and 28%, approaching the treatment-related mortality of bone marrow transplantation. 24 Furthermore, we have noted an association between prior splenectomy and grade II IV, but not grade III IV, acute GVHD. Although such an association has been noted in the past 25,26 this is the first time it has been shown in patients with MF and we await confirmation of this finding in larger groups of patients. Although patients who achieve CR may experience longterm survival, we have observed significant treatmentrelated morbidity and mortality. Patients with MF require more extensive transfusion support than other transplant recipients. Patients may continue to require transfusions of packed red blood cells for as long as 1 year after transplantation, even in the absence of major ABO blood group incompatibility. A recent review of the transfusion needs of 519 allogeneic SCT recipients treated at Princess Margaret Hospital demonstrated that patients received an average of U of packed red blood cells per day over the first 18 days after transplantation. 27 This is significantly less than the transfusion needs of the MF patients in this cohort ( U/day over the same time period) (Po.1). Cumulative treatment-related mortality was 48.3% over the course of the first year, with deaths because of the effects of the conditioning regimen, infection and GVHD predominating. The predominance of older patients with long-standing advanced disease and the high number of patients who received transplants from alternative donors in this cohort likely contributed to the high treatment-related mortality we have observed. Reports documenting the response of patients with MF to nonmyeloablative stem cell transplants suggest that this disease may be amenable to treatment with reducedintensity conditioning, 28 although patients treated in this way will continue to be at risk for GVHD and infection. The rate of recurrence of myeloproliferative disorders following non-myeloablative SCT is unknown at present. These results suggest that allogeneic SCT is a reasonable treatment approach for patients with advanced AMM and ET complicated by MF. No other therapeutic options have the potential to reverse fibrosis and restore normal hematopoiesis in this group of patients. Furthermore, prolonged disease-free survival may be a realistic goal for patients with MF and an HLA-compatible donor. Given the high treatment-related mortality we have observed and advanced age of patients with MF in general, exploration of novel treatment strategies, such as nonmyeloablative approaches to transplantation, may be advisable to reduce treatment-related mortality. References 1 Reilly JT. Pathogenesis and management of idiopathic myelofibrosis. Baillieres Clin Hematol 1998; 11: Mesa RA, Elliott MA, Tefferi A. Splenectomy in chronic myeloid leukemia and myelofibrosis with myeloid metaplasia. Blood Rev 2; 14: Smith BD, Moliterno AR. Biology and management of idiopathic myelofibrosis. Curr Opin Oncol 21; 13:
6 4 4 Popplewell L, Forman SJ. Allogeneic hematopoietic stem cell transplantation for acute leukemia, chronic leukemia and myelodysplasia. Hematol Oncol Clin North Am 1999; 13: Anderson JE, Sale G, Appelbaum FR et al. Allogeneic marrow transplantion for primary myelofibrosis and myelofibrosis secondary to polycythaemia vera or essential thrombocytosis. Br J Haematol 1997; 98: Singhal S, Powles R, Treleaven J et al. Allogeneic bone marrow transplantation for primary myelofibrosis. Bone Marrow Transplant 1995; 16: De Revel T, Giraudier S, Nedellec G et al. Allogeneic bone marrow transplantation for postpolycythemic myeloid metaplasia with myelofibrosis: a case report. Bone Marrow Transplant 1995; 16: Bullorsky EO, Shanley CM, Stemmelin G et al. Acute megakaryoblastic leukemia with massive myelofibrosis: complete remission and reversal of marrow fibrosis with allogeneic bone marrow transplantation as the only treatment. Bone Marrow Transplant 199; 6: Dokal I, Jones L, Deenmamode M et al. Allogeneic bone marrow transplantation for primary myelofibrosis. Br J Haematol 1989; 71: Rajantie J, Sale GE, Deeg HJ et al. Adverse effect of severe marrow fibrosis on hematological recovery after chemoradiotherapy and allogeneic bone marrow transplantation. Blood 1986; 67: Soll E, Massumoto C, Clift RA et al. Relevance of marrow fibrosis in bone marrow transplantation: a retrospective analysis of engraftment. Blood 1995; 86: Barosi G. Myelofibrosis with myeloid metaplasia: diagnostic definition and prognostic classification for clinical studies and treatment guidelines. J Clin Oncol 1999; 17: Murphy S, Peterson P, Iland H, Laszlo J. Experience of the Polycythemia Vera Study Group with essential thrombocythemia: a final report on diagnostic criteria, survival, and leukemic transition by treatment. Semin Hematol 1997; 34: Appelbaum FR, Dahlberg S, Thomas ED et al. Bone marrow transplantation or chemotherapy after remission induction in adults with acute non-lymphoblastic leukemia. Ann Intern Med 1984; 11: Santos GW, Tutschka PJ, Brookmeyer R et al. Marrow transplantation for acute nonlymphocytic leukemia after treatment with busulfan and cyclophosphamide. N Engl J Med 1983; 39: Storb R, Deeg HJ, Farewell V et al. Methotrexate and cyclosporine compared with cyclosporine alone for prophylaxis of acute graft-versus-host disease after marrow transplantation for leukemia. N Engl J Med 1986; 314: Przepiorka D, Weisdorf D, Martin P et al. Consensus conference on acute GVHD grading. Bone Marrow Transplant 1995; 15: Shulman HM, Sullivan KM, Weiden PL et al. Chronic graftversus-host syndrome in man. A long-term clinicopathologic study of 2 Seattle patients. Am J Med 198; 69: McDonald GB, Sharma P, Matthews DE et al. Venoocclusive disease of the liver following allogeneic bone marrow transplantation: diagnosis incidence and predisposing factors. Hepatology 1984; 4: Cancer Therapy Evaluation Program. Common Toxicity Criteria, Version 2. (CTC, v2.), publish date April 3, Dupriez B, Morel P, Demory JL et al. Prognostic factors in agnogenic myeloid metaplasia: a report on 195 cases with a new scoring system. Blood 1996; 88: Kaplan EL, Meier P. Non-parametric estimation from incomplete observations. J Am Stat Assoc 1958; 53: Guardiarola P, Anderson JE, Bandini G et al. Allogeneic stem cell transplantation for agnogenic myeloid metaplasia: a European Group for Blood and Marrow Transplantation, Societe Francaise de Greffe de Moelle, Gruppo Italiano per il Trapianto de Midollo Osseo and Fred Hutchinson Cancer Research Center collaborative study. Blood 1999; 93: Weinstein IM. Idiopathic myelofibrosis: historical review, diagnosis and management. Blood Rev. 1991; 5: Michallet M, Corront B, Bosson JL et al. Role of splenectomy on incidence and severity of acute graft-versus-host disease: a multicenter study of 157 patients. Bone Marrow Transplant 1991; 8: Ringden O, Nilsson B. Death by graft-versus-host disease is associated with HLA-mismatch, high recipient age, low marrow cell dose and splenectomy. Transplantation 1985; 4: Xenocostas A, Yee A, Wong CJ et al. Red blood cell transfusion requirements after allogeneic bone marrow transplantation: impact of the pre-transplant hemoglobin level on transfusion and early survival. Transfusion 23; 43: Devine SM, Hoffman R, Verma A et al. Allogeneic blood cell transplantation following reduced-intensity conditioning is effective therapy for older patients with myelofibrosis with myeloid metaplasia. Blood 22; 99:
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