Allogeneic Stem Cell Transplantation with Peripheral Blood Stem Cells Mobilized by Pegylated G-CSF
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1 Biology of Blood and Marrow Transplantation 12:63-67 (26) 26 American Society for Blood and Marrow Transplantation /6/126-2$32./ doi:1.116/j.bbmt Allogeneic Stem Cell Transplantation with Peripheral Blood Stem Cells Mobilized by Pegylated G-CSF Geoffrey R. Hill, 1,2 Edward S. Morris, 1,2 Madonna Fuery, 2 Cheryl Hutchins, 2 Jason Butler, 2 Andrew Grigg, 3 Andrew Roberts, 3 Ken Bradstock, 4 Jeffrey Szer, 3 Glen Kennedy, 2 James Morton, 2 Simon Durrant 2 1 The Queensland Institute of Medical Research, Herston, Queensland, Australia; 2 Bone Marrow Transplant Unit, Royal Brisbane Hospital, Brisbane, Queensland, Australia; 3 Bone Marrow Transplant Service, Royal Melbourne Hospital, Melbourne, Victoria, Australia; 4 Bone Marrow Transplant Service, Westmead Hospital, Sydney, New South Wales, Australia Correspondence and reprint requests: Geoffrey R. Hill, MD, Bone Marrow Transplantation Laboratory, Queensland Institute of Medical Research, 3 Herston Road, Herston, QLD 46, Australia ( geoffh@qimr.edu.au). Received October 6, 25; accepted March 1, 26 ABSTRACT Mobilization of stem cells with pegylated granulocyte colony-stimulating factor (peg-g-csf) modulates donor T- and natural killer T-cell (NKT-cell) functions, thus separating graft-versus-host from graft-versusleukemia disease in animal models. We report a phase I/II study that analyzed the feasibility of mobilizing stem cells from normal donors with peg-g-csf and the ability of these cells to restore hematopoiesis in allogeneic transplant recipients after myeloablative conditioning. Administration of 6 mg of peg-g-csf resulted in suboptimal stem cell mobilization, with a peak peripheral blood CD34 count of 29 5/ L. Apheresis 4 days after peg-g-csf yielded CD34 cells/kg recipient weight, and all donors required a second collection on day 5 to yield a total of CD34 cells/kg recipient weight. After escalation of the dose to 12 mg, the peak CD34 count was 99 11/ L and 12 of 13 donors collected sufficient stem cells for transplantation in a single apheresis ( CD34 cells/kg recipient weight). Late transient increases in serum hepatic transaminases were noted, but other side effects (predominantly bone pain) were otherwise similar to those seen in donors mobilized with standard G-CSF. Median neutrophil and platelet engraftments occurred on days 18 and 14, respectively, after transplantation and were identical to those seen with in recipients of grafts mobilized with standard G-CSF. With a median follow-up of 357 days, the incidence of grade II-IV acute graft-versus-host disease was 5% and there have been no relapses to date. Mobilization of stem cells with peg-g-csf in normal donors is feasible and 12 mg results in mobilization characteristics similar to those of standard G-CSF. 26 American Society for Blood and Marrow Transplantation KEY WORDS Stem cell mobilization Pegylated G-CSF Graft-versus-host disease INTRODUCTION Transplantation of peripheral blood stem cells mobilized by granulocyte colony-stimulating factor (G- CSF) has become standard practice in allogeneic transplantation. Despite the transfer of large numbers of donor T cells, the incidence of acute graft-versus-host disease (GVHD) is not increased, which is postulated to be the result of immunomodulation by G-CSF [1,2]. GRH is a Wellcome Trust Senior Overseas Research Fellow. Immunomodulation by G-CSF is complex and involves T-helper type 2 differentiation [3,4] and the induction of regulatory T and antigen-presenting cells [5-7]. We recently reported that mobilization with G-CSF protects against experimental GVHD in a dose-dependent fashion and that this effect is maximal after administration of pegylated G-CSF (peg-g-csf) [8]. In addition, peg-g- CSF activates donor natural killer T (NKT) cells and increases graft-versus-leukemia effects in experimental models [9]. We therefore initiated a phase I/II clinical trial to examine transplantation of peripheral blood 63
2 G. R. Hill et al. grafts mobilized by peg-g-csf and report on our initial experience in normal donors. METHODS Patient Accrual All recipients (and donors) receiving their first allogeneic stem cell transplants from an HLAmatched sibling after myeloablative conditioning and cyclosporine/methotrexate GVHD prophylaxis were eligible. Donors and recipients were required to fulfill standard criteria for minimum organ function and negative viral serology. Enrollment commenced in February 24. Protocols were approved by the institutional ethics committees and donors and recipients provided written informed consent. A cohort of 19 donors receiving stem cell mobilization with standard G-CSF over the period are included for comparison. These donor-recipient pairs did not fulfill the peg-g- CSF entry criteria, usually on the basis of conditioning regimen. Stem Cell Collections All donors received a single dose of peg-g-csf (Neulasta, Amgen, Thousand Oaks, Calif) at 6 mg subcutaneously on day. Full blood counts, biochemistry, and CD34 counts were monitored days 2-5 and 12 after peg-g-csf administration. Donors were harvested on day 4 by standard apheresis (Cobe Laboratories, Lakewood, Calif; 3 blood volumes). Target stem cell yield was CD34 cells/kg recipient ideal body weight. If CD34 cells/kg recipient ideal weight was not achieved in a single collection, a second collection was performed on day 5 and products were combined and infused on day. Data are based on recipient ideal body weight. Donors completed side effect questionnaires until full recovery and side effects were graded from (normal) to 1 (severe). The cohort of donors receiving stem cell mobilization with standard G-CSF received 1 g kg 1 d 1. Dose escalation to 12 mg was planned if stem cell mobilization with 6 mg of peg-g-csf was inferior to that seen with standard G-CSF. Transplantation Protocols Transplant recipients were conditioned with cyclophosphamide (6 mg/kg on days 5 and 4) and total body irradiation (TBI) (2 Gy twice daily on days 3 to 1) or with fludarabine (3 mg/kg on days 6 to 2) and melphalan (12 mg/kg on day 1). All recipients received cyclosporine (5 mg/kg on days 1 to 1 and then 3 mg/kg [ideal body weight]) adjusted to therapeutic institutional levels. Methotrexate was administered on day 1 (15 mg/m 2 ) and days 3, 6, and 11 (1 mg/m 2 ). G-CSF after transplantation was limited to recipients with delayed neutrophil recovery ( /L) on day 21. Supportive care was as previously described [1]. Evaluation and Definitions Stem cell products were analyzed as previously described [11]. Neutrophil engraftment was defined as occurring on the first of 3 days with a neutrophil count /L after the post-transplant nadir. Organ toxicities were graded using National Cancer Institute criteria. Platelet engraftment was defined as occurring on the first of 5 consecutive days with a platelet count /L without platelet transfusions. Acute GVHD was graded by Seattle criteria [12]. RESULTS AND DISCUSSION Donor Characteristics Donor characteristics are listed in Table 1 and side effects in those receiving 6 and 12 mg of peg-g-csf were similar (predominantly bone pain). White blood cell count peaked 2-3 days after the 6-mg dose of peg-g-csf and was significantly lower than in donors receiving 12 mg, which peaked later. Platelet nadirs were lowest in donors receiving 12 mg of peg-g-csf but remained at acceptable levels (Table 1 and Figure 1). Liver function changes were characterized by increases in serum alkaline phosphatase, which peaked on days 4-5 and correlated with the dose of peg-g- CSF. National Cancer Institute grade 2 toxicity was seen in 1 of 5 donors receiving the 6-mg dose and 7 of 13 receiving the 12-mg dose. Increases in alkaline phosphatase and lactate dehydrogenase were not significantly different between the 6- and 12-mg cohorts (Table 1). However, increases in alanine aminotransferase (ALT) were seen after stem cell collection, ie, 5-12 days after peg-g-csf administration. Of the 5 donors receiving the 6-mg dose, 2 had National Cancer Institute grade 1 toxicity and 1 had grade 2. Of the 13 donors receiving the 12-mg dose, 7 had grade 1 toxicity, 1 had grade 2, and 1 had grade 3. The donor with grade 3 toxicity also developed palpable splenomegaly, which was confirmed on ultrasound and was transient. Increased ALT, which occurred in 66% of donors, was also transient and returned to normal levels by a median of 24 days (range, 5-37) after peg-g-csf administration. There were also associated but less marked increases in aspartate aminotransferase in 25% of donors (median, 32; range, ; normal, 4) but no increases in serum bilirubin were seen. The mean increase in ALT in donors receiving 12 mg of peg-g-csf was higher than that in those receiving 6 mg (13 38 versus U/L; normal, 45 U/L). Although 1 donor receiving standard G-CSF over the same time period developed a grade 2 increase in ALT, this group was not routinely 64
3 Peg-G-CSF Mobilized Stem Cells for Allogeneic SCT Table 1. Donor Characteristics, Side Effects, and Graft Composition* Units (Normal Range) peg-g-csf (6 mg) peg-g-csf (12 mg) G-CSF (1 g/kg) (n 5) (n 13) (n 19) Donor characteristics Age, y 4 (28-5) 42 (23-62) 48 (14-65) Weight, kg 76 (63-8) 8 (6-115) 91 (53-126) Male:female 3:2 9:4 12:7 G-CSF total dose, g/kg 79 (75-95) 15 (14-2) 4 Side effects Maximal lower back pain (-1) 7 (4-8) 5 (-9) N/A Days of lower back pain 5 (3-9) 5 (-16) N/A Maximal headache (-1) 5 (6-8) 5 (-1) N/A Days of headache 5 (-1) 3 (-9) N/A Maximal myalgia (-1) 6 (-7) 3 (-8) N/A Days of myalgia 4 (-11) 4 (-1) N/A Maximal fatigue (-1) 6 (2-1) 5 (-9) N/A Days of fatigue 1 (4-18) 7 (-2) N/A Peak WBC, 1 9 /L (<1) 33 (28-4) 48 (37-7) 44 (26-83) Platelet nadir, 1 9 /L (15-45) 144 (124-15) 19 (7-178) 243 ( ) Peak ALP, U/L (4-11) 28 (118-28) 295 (19-434) 25 ( ) Peak LDH, U/L (11-25) 279 (199-47) 419 (322-89) 414 ( ) Peak ALT, U/L (<45) 43 (2-113) 71 (15-541) 26 (11-186) Cellular content of infused grafts Total nucleated cells/kg ( 1 8 ) CD34 /kg ( 1 6 ) CD4 /kg ( 1 6 ) CD8 /kg ( 1 6 ) *WBC indicates white blood cell count; ALP, alkaline phosphatase; LDH, lactate dehydrogenase; N/A, not assessed. Data expressed as median (range) or mean SE and compared by Mann Whitney U test. P.5. P.1, peg-g-csf 12 mg versus 6 mg. P.5, G-CSF versus peg-g-csf 6 mg. P.5, G-CSF versus peg-g-csf 6 and 12 mg. monitored after day 4, so late increases in ALT would not have been detected. We therefore monitored liver function on days 6 to 9 after standard G-CSF administration in the next 1 normal donors and observed grade 1 increases in ALT in 5% of individuals (median peak ALT, 48 U/L; range, 14-7), suggesting this effect is not peculiar to peg-g-csf. Nevertheless, grade 2 and 3 increases in ALT after administration of peg-g-csf have prompted us to exclude donors with abnormal liver function and restrict alcohol and paracetamol consumption during stem cell mobilization and for the week thereafter. Grade 1 increases in ALT were seen only in the subsequent cohort of 4 recipients. Stem Cell Products After mobilization with 6 mg of peg-g-csf, increases in CD34 counts were modest, peaking 3 days after administration (mean SE, 29 5/ L). Collection of CD34 stem cells on day 4 was suboptimal ( /kg recipient weight) and all patients required a second collection on day 5 (yielding /kg recipient weight), which, when combined with the day 4 collection, yielded a total of CD34 cells/kg recipient weight (Figure 1 and Table 1). Of the donors mobilized with standard G- CSF, 32% collected /kg recipient weight in a single collection on day 4. Because mobilization of stem cells with the 6-mg dose of peg-g-csf was significantly inferior to that seen with standard G- CSF (Figure 1), the dose was increased to 12 mg. At this dose, stem cell mobilization was robust, with stem cell counts peaking on day 4 at CD34 cells/ L of peripheral blood (mean SE). Twelve of 13 donors collected adequate numbers of CD34 cells for transplantation ( /kg recipient weight) in a single apheresis on day 4 ( /kg recipient weight) and 7 of 13 collections were only partly infused to maintain the numbers of CD34 cells transplanted at /kg recipient weight. The cellular content of infused grafts from donors mobilized with 12 mg of peg-g-csf was similar to that mobilized by standard G-CSF or 6 mg of peg-g- CSF (Table 1). Because of the superior mobilization with peg-g-csf at the 12-mg dose compared with standard G-CSF, the predicted rate of failure to mobilize would be expected to be similar to or lower than that seen with standard G-CSF. Recipient Characteristics, Engraftment, and Transplantation Outcome Characteristics of transplant recipients with assessable acute GVHD data (transplanted 1 days 65
4 G. R. Hill et al. A B WBC (x1 9 /L) Day post peg-g-csf 6mg 12mg blood CD34 + cells (/μl) Day post peg-g-csf Peg-G-CSF Peg-G-CSF Stem cell mobilization Stem cell collection Engraftment P<.15 P<.15 C D E P<.1 P=.13 Blood CD34 + cells (/μl) P<.2 P<.25 Graft CD34 + (x1 6 /kg) Day of engraftment peg-g-csf (6mg) peg-g-csf (12mg) G-CSF (1μg/kg/day) peg-g-csf (6mg) peg-g-csf (12mg) G-CSF (1μg/kg/day) 5 neutrophil platelet Figure 1. Analysis of stem cell mobilization, collection, and engraftment after G-CSF administration. Donors received peg-g-csf on day. (A) White blood cell and (B) CD34 counts were determined by automated analysis on days 2-5 and thereafter as described in Methods. Solid circles indicate 6 mg of peg-g-csf (n 5), and open circles represent 12 mg of peg-g-csf (n 13). Donors received peg-g-csf on day and CD34 counts were determined by flow cytometry in the (C) peripheral blood and (D) apheresis products on day 4 and thereafter. Thin dashed lines represent the lower threshold in stem cell grafts required for adequate collections and thick dashed lines represent the minimum acceptable CD34 number in stem cell products for transplantation with 6 mg of peg-g-csf (n 5), 12 mg of peg-g-csf (n 13), and 1 g kg 1 d 1 of standard G-CSF on days -3 (n 19). E, Neutrophil and platelet engraftments after transplantation of grafts mobilized by peg-g-csf (n 14). Data were compared by Mann Whitney U test. previously) are presented in Table 2. The mean number of CD34 cells actually transplanted from peg-g- CSF mobilized donors was /kg recipient weight and the 6- and 12-mg cohorts are considered together for engraftment purposes because the final number of CD34 cells infused to donors was adequate in both groups. Recipients transplanted with stem cell grafts mobilized with peg-g-csf achieved neutrophil and platelet engraftment at a median of 18 and 14 days, respectively, after transplantation (Table 2), with stable engraftment maintained at a median follow-up of 357 days (range, ) in surviving recipients. The median of neutrophil and platelet engraftment for 9 recipients receiving allogeneic stem cell grafts mobilized by standard G-CSF after cyclophosphamide/total body irradiation conditioning over the same period was 18 days (range, 12-24) and 13 days (range, 7-25), respectively. Further, the median number of red blood cell and platelet transfusions for these recipients was similar at 8 (range, 2-27) and 9 (range, 2-15), respectively. Seven recipients (5%) developed at least grade II acute GVHD (Table 2). Four recipients developed severe (grade III/IV) acute GVHD (29%) involving the gastrointestinal tract that was refractory to steroid therapy in 3 cases, requiring therapy with antithymocyte globulin. Three of these recipients died from GVHD 52, 89, and 145 days after transplantation. 66
5 Peg-G-CSF Mobilized Stem Cells for Allogeneic SCT Table 2. Recipient Characteristics and Outcome After Transplantation* Recipients of peg- G-CSF Grafts (n 14) Recipient characteristics Age, median (range) 46 (21-57) Male:female 1:4 Disease AML 9 ALL 2 CML 2 CLL 1 Conditioning Cy/TBI 13 Flu/Mel 1 Disease status Early 9 Advanced 5 Engraftment Neutrophil recovery, median (range) 18 (11-22) Platelet recovery, median (range) 14 (8-27) RBC transfusions, median (range) 5 (-33) Platelet transfusions, median (range) 4 (1-19) Acute GVHD Grade, n (%) -I 7 (5%) II 3 (21%) III/IV 4 (29%) Grade II-IV organ involvement, n (%) Skin 7 (5%) Gut 5 (36%) Liver 4 (29%) Overall survival, n (%) 11 (79%) Hematologic relapse (%) Median days of follow-up (range)# 357 ( ) *AML indicates acute myoblastic leukemia; ALL, acute lymphoblastic leukemia; CML, chronic myoblastic leukemia; CLL, chronic lymphoblastic leukemia; Cy/TBI, cyclosporine/total body irradiation; Flu/Mel, fludarabine/melphalan; RBC, red blood cell. First chronic phase. As defined in Methods. Number of units. Four units of multidonor platelets. #Follow-up is for surviving patients. The incidence of grade II-IV acute GVHD and grade III/IV acute GVHD at The Royal Brisbane unit was previously reported as 54% and 43%, respectively, in this setting [1]. No recipients have developed hematologic relapse to date. Mobilization of stem cells with peg-g-csf in normal donors is feasible. Further data are required to more closely analyze the effect of peg-g-csf on donor liver function and the ability of these stem cell grafts to induce GVHD and graft-versus-leukemia effects. REFERENCES 1. Bensinger WI, Martin PJ, Storer B, et al. Transplantation of bone marrow as compared with peripheral-blood cells from HLA-identical relatives in patients with hematologic cancers. N Engl J Med. 21;344: Morris ES, Macdonald KP, Hill GR. Stem cell mobilization with G-CSF analogs: a rational approach to separate GVHD and GVL? Blood. Dec. 25; doi:1.1182/blood Pan L, Delmonte J, Jalonen CK, Ferrara JLM. Pretreatment of donors with granulocyte colony-stimulating factor polarizes donor T lymphocytes toward type 2 cytokine production and reduces severity of experimental graft versus host disease. Blood. 1995;86: Franzke A, Piao W, Lauber J, et al. G-CSF as immune regulator in T cells expressing the G-CSF receptor: implications for transplantation and autoimmune diseases. Blood. 23;12: Rutella S, Pierelli L, Bonanno G, et al. Role for granulocyte colony-stimulating factor in the generation of human T regulatory type 1 cells. Blood. 22;1: Fugier-Vivier IJ, Rezzoug F, Huang Y, et al. Plasmacytoid precursor dendritic cells facilitate allogeneic hematopoietic stem cell engraftment. J Exp Med. 25;21: MacDonald KP, Rowe V, Clouston A, et al. Cytokine expanded myeloid precursors function as regulatory antigen-presenting cells and promote tolerance through IL-1 producing regulatory T cells. J Immunol. 25;174: Morris ES, MacDonald KPA, Rowe V, et al. Donor treatment with pegylated G-CSF augments the generation of IL-1 producing regulatory T cells and promotes transplant tolerance. Blood. 24;13: Morris ES, Macdonald KP, Rowe V, et al. NKT cell-dependent leukemia eradication following stem cell mobilization with potent G-CSF analogs. J Clin Invest. 25;115: Morton J, Hutchins C, Durrant S. Granulocyte-colony-stimulating factor (G-CSF)-primed allogeneic bone marrow: significantly less graft-versus-host disease and comparable engraftment to G-CSF-mobilized peripheral blood stem cells. Blood. 21;98: Sutherland DR, Anderson L, Keeney M, Nayar R, Chin-Yee I. The ISHAGE guidelines for CD34 cell determination by flow cytometry. International Society of Hematotherapy and Graft Engineering. J Hematother. 1996;5: Przepiorka D, Weisdorf D, Martin P, et al Consensus conference on acute GVHD grading. Bone Marrow Transplant. 1995;15:
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