ORIGINAL ARTICLE. HJ Im 1, KN Koh 1, JK Suh 1, SW Lee 1, ES Choi 1, S Jang 2, SW Kwon 2, C-J Park 2 and JJ Seo 1
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1 Bone Marrow Transplantation (2016) 51, Macmillan Publishers Limited, part of Springer Nature. All rights reserved /16 ORIGINAL ARTICLE Haploidentical HCT using an αβ T-cell-depleted graft with targeted αβ + cells by add-back after a reduced intensity preparative regimen containing low-dose TBI HJ Im 1, KN Koh 1, JK Suh 1, SW Lee 1, ES Choi 1, S Jang 2, SW Kwon 2, C-J Park 2 and JJ Seo 1 Between 2012 and 2015, 42 pediatric patients underwent haploidentical hematopoietic cell transplantation using an αβ + T-cell-depleted graft with targeted αβ cells at /kg by add-back; 31 had hematologic malignancy (HM), 8 had non-malignant disease (NM) and 3 had solid tumors. All patients received uniform reduced-intensity conditioning with fludarabine, cyclophosphamide, rabbit anti-thymocyte globulin and low-dose TBI. All 42 patients achieved neutrophil engraftment at a median of 10 days. The cumulative incidences (CIs) of grade II and grade III acute GvHD were 31 ± 7.1% (SE) and 12 ± 5.0%, respectively, and 1-year CI of chronic GvHD was 15 ± 5.8%. One patient died of CMV pneumonia, leading to transplant-related mortality (TRM) of 2.6 ± 2.5%. Sixteen patients relapsed and 11 died of disease. At a median follow-up of 19 months (range, 5 43 months), the estimated 2-year event-free survival for NM and HM were 88 ± 11.7 and 50 ± 10.1%, respectively. Our study demonstrated that haploidentical hematopoietic cell transplantation after ex vivo depletion of αβ + T cells with targeted dose noticeably reduced the graft failure rate and TRM in pediatric patients and could be applied to patients lacking a suitable related or unrelated donor. Bone Marrow Transplantation (2016) 51, ; doi: /bmt ; published online 9 May 2016 INTRODUCTION Recent advances with effective ex vivo depletion of T cells or unmanipulated in vivo regulation of T cells, better supportive care and optimal conditioning regimens have significantly improved the outcomes of haploidentical hematopoietic cell transplantation (HHCT). The ex vivo techniques to remove T cells have evolved from the selection of CD34 + hematopoietic stem cell progenitors to the depletion of CD3 + cells and, more recently, the depletion of αβ + T cells. Compared with the positive selection of CD34 + cells, direct depletion of CD3 + cells has the advantage of increased numbers of natural killer cells, monocytes and other immunomodulating cells with improved outcomes. 1 3 Moreover, preliminary reports on the new method of αβ + T-cell depletion showed further improved outcomes for T-cell-depleted haploidentical transplants. 4,5 Depletion of αβ + T cells produces grafts containing many γδ + lymphocytes and other effector cells. While αβ + T cells are known to be associated with the initiation of GvHD, γδ + T cells can enhance immune reconstitution and are not implicated in GvHD. 6 Recently, we reported our experience with HHCT using a CD3-depleted graft. 7 Since 2012, we have initiated HHCT using ex vivo depletion of αβ + T cells with targeted αβ cells at /kg after add-back. Here, we report our prospective results using αβ-depleted grafts in HHCT for children and adolescents with malignant or non-malignant disease. MATERIALS AND METHODS Patients Between May 2012 and June 2015, 42 children and adolescents underwent HHCT using αβ + T-cell-depleted PBSC with targeted αβ cells at /kg after add-back. All transplantation protocols were approved by the Institutional Review Board of Asan Medical Center and registered at (NCT ). All patients and donors provided written informed consent. HLA typing and donor evaluation HLA typing was performed by using a high-resolution molecular method for HLA-A, -B, -C and DRB1. KIR genotyping was determined using a KIR typing kit (Miltenyi-BioTec, Bergisch-Gladbach, Germany). Anti-HLA antibodies were measured using a Luminex-based single antigen bead assay (One Lambda, Canoga Park, CA, USA). Conditioning regimens and GvHD prophylaxis All 42 patients underwent a uniform reduced-intensity conditioning regimen consisting of fludarabine (180 mg/m 2 ), cyclophosphamide (100 mg/kg), rabbit anti-thymocyte globulin (thymoglobulin; 2 mg/kg at D-8 and 1 mg/kg at D-7 for malignant disease and 2.5 mg/kg at D-8 through D-6 for non-malignant disease) and low-dose TBI (200 cgy/fraction at D-6 through D-4 for malignant disease and at D-5 and D-4 for non-malignant disease). To prevent GvHD, tacrolimus and mycophenolate mofetil were administered from the day of PBSC infusion. Mycophenolate mofetil was administered orally at a dose of 15 mg/kg twice a day and discontinued on day +28. Tacrolimus was continued until day +90. After day +90, the tacrolimus dose was gradually reduced by 5% per weeks and the drugs were discontinued at approximately 8 months after grafting if the patient was not under treatment for GvHD. Stem cell collection and graft manipulation by T-cell depletion All donors received G-CSF for a minimum of four consecutive days and PBSCs were collected on days 1 and 0. The αβ + T cells were depleted by negative selection using the CliniMACS system (Miltenyi-BioTec). The final 1 Department of Pediatrics, University of Ulsan College of Medicine, Asan Medical Center, Seoul, Korea and 2 Department of Laboratory Medicine, University of Ulsan College of Medicine, Asan Medical Center, Seoul, Korea. Correspondence: Professor HJ Im, Department of Pediatrics, University of Ulsan College of Medicine, Asan Medical Center, 88-1 Olympic-ro 43-gil, Songpa-gu, Seoul , Korea. hojim@amc.seoul.kr Received 16 December 2015; revised 19 March 2016; accepted 22 March 2016; published online 9 May 2016
2 1218 doses of αβ + T cells in the infused graft were adjusted to /kg by adding back αβ + T cells from the negative selection product. All patients received rituximab post-hhct to deplete B cells at approximately day +28 or earlier if EBV was detected with PCR. Supportive care Patients were given antibiotics for bacterial prophylaxis and micafungin for fungal prophylaxis. For CMV prophylaxis, ganciclovir (5 mg/kg twice per day) was used prior to HHCT and foscarnet (60 mg/kg/day) after transplantation and up until engraftment. After engraftment, ganciclovir (5 mg/kg/day) or valganciclovir (25 mg/kg/day) was administered until 100 days post-transplantation and recovery of CD4 + cell numbers (4100/μL). Beginning on day 4, patients received G-CSF (5 μg/kg/day) until an ANC of 2000/μL was achieved for three consecutive days. Post-transplant assessment Donor engraftment was determined by using DNA-based STR assays from whole-blood samples on days 14, 30, 60, 90, 180 and 360 post transplant. Full donor chimerism was defined as 95% donor cells. For hematologic malignant disease cases, we performed bone marrow examination at 1, 3, 6, 9 and 12 months post-transplant. Viral surveillance included weekly screening for CMV using PCR and antigenemia assays and weekly screening for EBV using PCR. Preemptive therapy with ganciclovir was initiated when positive results were obtained in PCR and antigenemia assays for CMV. Acute GvHD was graded according to standard criteria and chronic GvHD was defined as absent, limited or extensive. 8,9 Statistical analysis Cumulative incidence (CI) was used to summarize the probability of GvHD, non-relapse mortality, relapse and CMV reactivation/disease using a competing risks model. Relapse was a competing risk for NRM, and death was a competing risk for engraftment, GvHD, NRM and relapse. The Kaplan Meier method was used to calculate the probability of overall survival and event-free survival. The overall survival end point was death and event-free survival end points were death or relapse. The date of the last follow-up for all patients was 30 November All statistical analyses were performed with STATA version 11.0 (Stata Corp LP, College Station, TX, USA) and SPSS version 21.0 (Statistical Package for the Social Sciences; IBM, Armonk, NY, USA). RESULTS Patient characteristics Of the 42 patients, 25 were male. The median age at the time of transplantation was 13.2 years (range, years). Characteristics of the patients and donors are summarized in Table 1. Thirty-one patients had hematologic malignancy, seven patients had acquired severe aplastic anemia, one had Wiskott-Aldrich syndrome and three had had solid tumors (two rhabdomyosarcoma and one Ewing sarcoma). Detailed profiles of patients with hematologic malignancies are shown in Table 2. All donors were fully haploid and had two mismatched HLA loci at HLA-A, -B and DRB1. Donors were mothers in 19 cases, fathers in 9 cases and siblings in 14 cases. Depletion data and graft composition The median log depletion of αβ + T cells was 3.8 (range, ). After depletion, the number of αβ + T cells was adjusted to target at /kg with add-back. The αβ + T cells before and after depletion and the αβ + T cells/kg before and after add-back are shown in Figure 1. Graft compositions are shown in Table 1. Engraftment All 42 patients achieved neutrophil engraftment at a median of 10 days (range, 9 17 days) after HHCT, and 39 patients achieved platelet engraftment at a median of 15 days (range, days). Table 1. Characteristics of the patients and donors Number of patients 42 Age at transplant (years) Median (range) 13.2 ( ) Disease Hematologic malignancy 31 SAA 7 WAS 1 Rhabdomyosarcoma 2 Ewing sarcoma 1 Donors Mother 19 Father 9 Sibling 14 Anti-HLA antibody No antibody 16 Non-DSA 18 DSA a 8 Donor KIR haplotype (evaluated) (30) A 11 B 19 CMV serostatus, recipient/donor Negative/negative 0 Negative/positive 2 Positive/negative 5 Positive/positive 35 Duration of CMV prophylaxis (days) Median (range) 36 (15 103) Graft composition (cells/kg BW) CD34 + cell ( ) CD3 + T cells ( ) CD3 + αβ + T cells ( ) CD3 + γδ + T cells ( ) B cells ( ) NK cells ( ) Abbreviations: DSA = donor-specific antibodyl; SAA = severe aplastic anemia; WAS = Wiskott-Aldrich syndrome. a Two had antibodies against HLA class I antigen and four against HLA class II and two against both HLA I and II. The median DSA level was 1280 mean fluorescence intensity. Chimerism data For all 16 relapsed patients, their STR assay with peripheral blood performed at least 1 month prior to relapse showed more than 99% donor chimerism. Only one patient had 2% of recipientderived cells at 2 weeks prior to planned bone marrow examination, which confirmed marrow relapse. One patient with Wiskott-Aldrich syndrome showed mixed chimerism, ranging from 38 to 49% of donor cells, with stable platelet counts. The remaining 25 patients showed complete donor chimerism. Acute and chronic GvHD Of 42 patients, 13 developed grade II acute GvHD at a median of 28 days (range, 11 41). Eight patients had grade II, four had grade III and one had grade IV. The CIs of grade II and grade III acute GvHD were 31± 7.1% (SE) and 12 ± 5.0%, respectively. Forty-one patients were evaluated for chronic GvHD. Chronic GvHD developed in seven patients (limited in four, extensive in three), giving an estimated 1-year probability of 15 ± 5.8%. Two patients remained on immunosuppressants: one had bronchiolitis obliterans organizing pneumonia and the other had liver GvHD at the time of report. There were no GvHD-related deaths at last follow-up. Bone Marrow Transplantation (2016) Macmillan Publishers Limited, part of Springer Nature.
3 Immune reconstitution The immune reconstitution of all 42 patients who had sustained stable engraftment was evaluated (Figure 2). The NK cell recovery was fast and reached a normal value within 90 days post transplant. However, CD4 + T-cell recovery was delayed and did not reach donor levels by day 180. At day 14 after HHCT, CD3 + T cells predominantly consisted of γδ + T lymphocytes, with a median of 76.8% (range %). The γδ T-cell population then gradually decreased to 46% of CD3 + cells at day 28 post transplant, while the percentage of αβ T cells gradually increased. Infections CMV reactivation occurred in 13 patients at a median of 38 days (range, ) after HHCT, giving a CI of 34 ± 8.0%. One patient with severe aplastic anemia developed CMV reactivation at day Table 2. Profiles of 31 patients with hematologic malignancies Number of patients Previous allogeneic HCT ALL CR1 with t(9;22) 2 (1) 0 CR1 with t(9;11) 1 (1) 0 CR2 3 2 CR3 1 1 AML CR1 7 0 CR2 3 1 Active disease 4 2 MPAL CR3 1 0 Active disease 1 1 MDS-RCC 4 1 JMML 2 0 NHL CR2 1 0 CR3 1 0 Abbreviations: ALL = acute lymphoblastic leukemia; AML = acute myeloid leukemia; JMML = juvenile myelomonocytic leukemia; MDS = myelodysplastic syndrome; MPAL = mixed phenotype acute leukemia; NHL = non- Hodgkin s lymphoma; RCC = refractory cytopenia of childhood; ( ) = number of patients with induction failure , and died of CMV pneumonia at day This patient was seropositive for CMV, while the donor was seronegative for CMV. EBV reactivation occurred in 23 patients at a median of 34 days (range, ) post-transplantation. None developed post-transplant lymphoproliferative disorder. Hemorrhagic cystitis caused by the BK virus occurred in 10 patients at a median of 35 days (range, 7 90) post transplant, but all recovered completely after supportive care. One patient developed a disseminated tuberculosis infection and two patients developed invasive fungal infections that were successfully treated. No other cases of serious bacterial or fungal infections occurred during the study period. Transplant-related mortality One patient, who received HSCT from his sister for severe aplastic anemia, died of CMV pneumonia at 133 days post transplantation. The CI of transplant-related mortality (TRM) at 1 year post transplant was 2.6 ± 2.5%. Relapse As of November 2015, 16 patients (6 ALL, 6 AML, 1 MPAL, 1 NHL and 2 rhabdomyosarcoma) relapsed at a median of +134 days (range, days). Patients who had active disease at the time of HHCT or had relapse after a previous allogeneic transplant were defined as high risk, and patients who received HHCT in any remission without prior HSCT were defined as low risk. Five out of 14 patients with AML and 3 out of 7 with ALL were high risk. One patient of nine with LR-AML and two of four patients with LR-ALL experienced relapse, whereas all eight high-risk patients (five with AML and three with ALL) relapsed (Figure 3). Among 16 patients who relapsed after HHCT, 11 died of disease and 5 were alive at the time of report, leading to a 26 ±14.9% survival rate at 1 year after relapse. Donor lymphocyte infusions Of the 16 patients who relapsed after HHCT, 6 received donor lymphocyte infusion at a median of 11 days (range, 1 43 days) after relapse. Of these six patients, two patients received only one dose of donor lymphocyte infusion at CD3 + cells/kg and four patients received multiple donor lymphocyte infusions with escalating doses of CD3 + cells, ranging from to CD3 + cells/kg x /kg x 10 6 /kg x 10 5 /kg x 10 4 /kg 10 4 αβ + T cells before depletion αβ + T cells after depletion αβ + T cells/kg before add-back αβ + T cells/kg after add-back Figure 1. Depletion using anti-tcrαβ monoclonal antibody Macmillan Publishers Limited, part of Springer Nature. Bone Marrow Transplantation (2016)
4 CD3 + cells CD4 + cells αβ+ Τ cells γδ+ Τ cells CD56 + cells Cells/μL Months after transplantation Figure 2. Immune reconstitution of subsets of lymphocytes after HHCT. A full color version of this figure is available at the Bone Marrow Transplantation journal online % (HR-ALL, n =3 & HR-AML, n =5) % ± 11.7% % (LR-ALL, n =4) 0.8 Cumulative incidence Event free survival % ± 10.1% % (LR-AML, n =9) 0.2 Non-malignant disease (n =8) Hematologic malignancy (n =31) Years after transplantation Figure 3. Cumulative incidence of relapse in patients with ALL and AML according to the risk group. Risk group stratification: high risk (HR) for patients with active disease at the time of HHCT or history of relapse after allogeneic HSCT, low risk (LR) for patients in any remission at the time of HHCT without history of previous allogeneic HSCT. Second transplantation for relapse Four relapsed patients received second transplantations at a median of 82 days (range, days) post relapse. Two patients died after another relapse. One patient with AML survived in CR months after the second HHCT, and the remaining patient with AML survived in CR +1.8 months after the second HHCT. Survival At a median follow-up of 19 months (range, 5 43 months), the estimated 2-year event-free survivals for non-malignant disease and hematologic malignancy were 88 ± 11.7 and 50 ± 10.1%, respectively (Figure 4). Of three patients with solid tumors, two Figure Years after transplantation Event-free survival. with rhabdomyosarcoma died of disease, while one patient with Ewing sarcoma survived in continuing CR 28.2 months after HHCT. DISCUSSION In our current prospective study, we demonstrated that HHCT using ex vivo αβ + T-cell-depleted grafts is a realistic treatment modality with a favorable early post-transplant outcome in children and adolescents with malignant or non-malignant disease. A uniform, reduced intensity preparative regimen containing low-dose TBI was applied. The number of αβ + T cells was targeted at /kg after add-back from the negative selection product, and all patients received tacrolimus and mycophenolate mofetil to prevent GvHD. The most relevant findings of our study are excellent engraftment and low TRM. A higher dose of αβ cells in the graft by add-back is a unique feature of our transplant procedure. Because we could not be sure Bone Marrow Transplantation (2016) Macmillan Publishers Limited, part of Springer Nature.
5 that a certain fixed dose was optimal, we adopted a target range rather than a target point. Furthermore, it was difficult, in practice, to target a fixed T-cell dose. Although several studies have suggested beneficial roles of γδ T cells in the context of hematopoietic cell transplantation, reports of clinical experiences are still very limited. 6,10 15 There have been several reports on HHCT in pediatric patients. 4,5,7,16 18 In our current study, all 42 patients achieved stable engraftment early post transplant at a median of 10 days. No patient experienced graft failure (GF), including late GF. Our previous study on HHCT using CD3-depleted grafts showed that 7 out of 28 patients experienced GF. 7 GF can be affected by many factors such as disease, prior therapy, conditioning regimen, T-cell dose, CD34 cell dose and T-cell depletion technique. 3,19 23 A matched comparison between the present study and our prior study using CD3- depleted grafts is difficult because stem cell dose, proportion of patients with NM and proportion receiving low-dose TBI are somewhat different between the two studies. Recent studies reported that a GF rate after αβ-depleted HHCT for pediatric patients ranged from 12 to 16.2%. 5,16 GvHD is one of the major limitations in HHCT and a major cause of NRM. Two recent studies on αβ-depleted HHCT reported CIs of acute grade 3GvHD as 0 and 15%, respectively. 5,16 In our present study, the incidences of acute and chronic GvHD were acceptable; notably, no patient died of GvHD. Only one patient died of a cause other than relapse in our present study (CMV pneumonia). This patient was CMVseropositive, while the donor was seronegative. Several reports have suggested negative impacts on survival if a CMV-negative donor is selected for a CMV-seropositive recipient. 24 A recent report also showed that CMV-negative donor/cmv-positive recipient cases were at a higher risk for incomplete response to antiviral therapy. 25 Therefore, we would select CMV-seropositive donors for seropositive patients in future trials. TRM was quite low (2.6%) in the present study. Recent reports on αβ-depleted HHCT in children with malignant or nonmalignant disease revealed low TRM rates of less than 10%. 5,16 Relapse was the major treatment failure in our present series. In studies of HHCT using αβ- or CD3-depleted grafts for pediatric patients with malignant disease, the major cause of death was relapse, especially in patients with advanced disease. 5,17 In our present study, only one of nine patients with AML who received a first HHCT relapsed. In contrast, all eight patients with acute leukemia who received HHCT while not in CR and/or received subsequent HHCT relapsed. Three of four patients with ALL who had neither active disease nor previous transplantation experienced relapse. At the present time, we cannot draw any firm conclusions regarding the efficacy of HHCT for pediatric ALL due to the small number of patients with ALL. Of three patients with solid tumors, one with Ewing sarcoma survived in CR for more than 2 years post transplant. Schlegel et al. 26 reported two patients with Ewing sarcoma who survived in long-term remission. However, allogeneic HSCT for solid tumors is still an experimental approach, and further studies are required to evaluate the efficacy of HHCT for solid tumors. In our current study, the dose of αβ + T cells was targeted at a rather higher number by add-back due to the concern regarding a higher GF rate based on our previous HHCTs using CD3-depleted grafts. 7 Our previous study with CD3-depleted HHCT showed a rather high incidence of GF in the early period of the study; therefore, we modified the targeted dose of T cells in different ranges to improve the outcomes. Another practical issue was that the reduction of T cells is less effective with the CD3-depletion method and frequently leads to residual T cells in the graft that exceed the threshold of /kg, requiring immunosuppressive drugs to prevent GvHD. We gradually reduced the targeted dose of T cells from /kg to /kg to decrease the risk of severe GvHD and ensure stable engraftment. Based on our 1221 previous experience with CD3-depleted grafts, the present study used αβ T-cell-depleted grafts with a targeted dose of αβ cells at /kg by add-back of αβ T cells from the negative selection product. We speculate that the higher T-cell dose used in the current trial is at least partly responsible for the reduced rate of GF without increasing the risk of severe GvHD. Given the excellent depletion efficacy of the protocol using anti-tcrαβ monoclonal antibody in this study and considering the cost and possible adverse effects of immunosuppressants, pharmacological prophylaxis to prevent GvHD will not to be used in future trials. Although our present study was prospectively conducted with a uniform preparative regimen and a targeted dose of T cells, there were several limitations, including a small number of patients, heterogeneous disease and a short follow-up. Our targeted and ranged T-cell dose-strategy improved the outcomes of ex vivo T-cell-depleted HHCT, although our protocol requires several modifications to develop a reasonable haploidentical transplant protocol. In addition, patients who had active disease or relapsed after previous transplantation showed poor outcomes, necessitating further treatment strategies such as cellular therapy based on γδ T cells or other immune cells. Furthermore, it is not certain whether using a fraction of T cells labeled with anti-tcr-α/β for add-back affects alloreactivity. In conclusion, HHCT after ex vivo depletion of αβ + T cells with a targeted dose noticeably reduced the graft failure rate and TRM in pediatric patients with malignant and non-malignant disease. This treatment modality could be applied for pediatric patients who have a transplantation-curable disease but lack a suitable related or unrelated donor. CONFLICT OF INTEREST The authors declare no conflict of interest. ACKNOWLEDGEMENTS This study was supported by a grant ( ) from the Asan Institute for Life Sciences, Seoul, Korea. REFERENCES 1 Lang P, Schumm M, Greil J, Bader P, Klingebiel T, Muller I et al. A comparison between three graft manipulation methods for haploidentical stem cell transplantation in pediatric patients: preliminary results of a pilot study. Klin Padiatr 2005; 217: Bethge WA, Faul C, Bornhauser M, Stuhler G, Beelen DW, Lang P et al. Haploidentical allogeneic hematopoietic cell transplantation in adults using CD3/CD19 depletion and reduced intensity conditioning: an update. Blood Cells Mol Dis 2008; 40: Handgretinger R, Chen X, Pfeiffer M, Mueller I, Feuchtinger T, Hale GA et al. Feasibility and outcome of reduced-intensity conditioning in haploidentical transplantation. 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