Double cord blood transplantation

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1 DCTH REVIEW Double cord blood transplantation R. Angarano, I. Donnini, B. Bartolozzi, A. Bosi Ematologia, Azienda Ospedaliera Universitaria Careggi, Università di Firenze, Italy SUMMARY In the last twenty years, the possibilities for transplantation have increased considerably with the introduction of alternative stem cell sources such as cord blood. The biggest benefits are the increase in availability of cord blood and the possibility to transplant units with more than one human leukocyte antigen mismatch, even if the dose cell limitation is critical, especially in adult transplants. The use of double cord blood units is one of the potential strategies that seem to overcome the cell dose limitation, improving engraftment and final transplant outcome. INTRODUCTION Hematopoietic stem cell transplantation (HSCT) using peripheral blood, cord blood, or bone marrow is used to treat a wide variety of genetic and immunological disorders and hematologic and solid organ malignancies (1). Cord blood (CB) has been increasingly used in the last ten years as an alternative source of hematopoietic Key words: allogeneic transplantation, double cord blood transplantation, graft-versus-host disease, total nucleated cells, human leukocyte antigen matching. Correspondence: Alberto Bosi Ematologia, Università degli Studi di Firenze U.O. di Ematologia, Azienda Ospedaliera Careggi Largo Brambilla, 3 - Firenze, Italy stem cells (HSC) for transplant. The presence of relatively mature hematopoietic progenitor cells (HPC) in human umbilical cord blood (UCB) was demonstrated by Knudtzon in 1974 (2). About ten years later, Ogawa and colleagues documented the presence of primitive HPC in UCB (3). However, it was not until 1989 that experimental and clinical studies were published indicating that human UCB could be used in clinical settings. Broxmeyer et al. showed experimental evidence that UCB was a rich source of hematopoietic stem/progenitor cells (HSPC) (4), and in the same year Gluckman et al. reported the first hematopoietic cell transplant in which UCB from an human leukocyte antigen (HLA)-identical sibling donor was used as a source of hematopoietic cells in a child with Fanconi anemia (5). Since then, there has been a growing interest in the use of UCB as an alternative source of HSPC for transplantation.

2 114 R. Angarano, et al. The biggest benefits are the increased availability of cord blood and the possibility of transplanting units with more than one HLA mismatch, even if the dose cell limitation is critical, especially in adult transplants. The experience gained and advances in supportive care have led to an improvement in outcomes after UCB transplantation (UCBT). In the setting of myeloablative conditioning regimens, large retrospective analyses showed comparable outcomes in UCBT and adult unrelated donor peripheral blood stem cell or bone marrow (BM) transplantation for adult patients with hematologic malignancies (6). Important advantages of UCB include a low incidence of graft-versus-host disease (GVHD), despite a high degree of HLA mismatch (7-10); acute GVHD occurs with lower frequency after UCBT compared with that observed after HLAmatched marrow from unrelated donors (11). Retrospective and prospective studies have shown that unrelated donor UCBT: 1. reconstitutes hematopoiesis and achieves sustained engraftment, but with delayed myeloid recovery; 2. is associated with a low incidence of GVHD; 3. does not result in a higher relapse risk and has similar survival rates to other sources of allogeneic HSCT. Because GVHD has been linked to relapse (12), there were initial concerns regarding the graft-versus-leukemia (GVL) potency of UCB. However, this has largely been resolved by single institution and registry studies, demonstrating a similar relapse risk compared with other HSC sources, including BM and PB (6, 12-14). Several studies have shown that cell dose is a critical determinant of hematopoietic recovery, transplant-related mortality (TRM), and overall survival after UCB transplant, which translates into increased risk of graft failure (15), delayed hematopoietic engraftment (13-16), and delayed immune reconstitution (17-18). Almost all series concerning UCBT in children and adults from unrelated donors have demonstrated the profound impact of cell dose, measured as pre-freeze or infused total nucleated cells (TNC), colony-forming cells, and CD34+ cells on engraftment, transplant-related events, and survival. Transplantation of a single UCB unit containing a prefreeze cell dose of 2.5x10 7 nucleated cells per kilogram, or an infused CD34 cell dose of 1.7x10 5 nucleated cells per kilogram, has been associated with poor engraftment, high non-relapse mortality (NRM) and poor survival (19). The cumulative incidence of non-engraftment after UCB transplantation varies from 10% to 20% and the median time to neutrophil recovery varies from 22 to 27 days. There is growing consensus that a UCB cell dose of 2.5x10 7 /kg represents the threshold of cryopreserved nucleated cells necessary for consistent engraftment (8, 9, 14). Although this cell dose is achievable with a single UCB unit for children, it is often not possible for adult recipients. Many different approaches have been explored to improve the engraftment. Examples include injecting cord blood cells directly into the bone marrow (20), in vivo o ex vivo amplification of cord blood cells (21, 22), use of reduced intensity conditioning (RIC) regimen (23, 25), co-infusion with a haploidentical T-cell depleted graft (26, 27)

3 Double cord blood transplantation 115 or mesenchymal stem cells (28), and use of double unit UCB transplantation (29). DOUBLE CORD BLOOD TRANSPLANTATION Given that cell dose and HLA disparities are important and independent factors associated with outcomes, it has been suggested that both factors interact mutually on engraftment and on other outcomes. Thus, a higher cell dose in the graft could partially overcome the negative impact of HLA for each level of HLA disparity, but this hypothesis has not been yet fully demonstrated. 18 The use of double cord blood units is one of the potential strategies that seems to overcome the cell dose limitation, improving engraftment and final transplant outcome. The method of transplanting 2 partially HLAmatched UCB units to overcome the cell-dose barrier was pioneered at the University of Minnesota (24, 29) and adopted by others to extend the application of UCB transplantation. Multiple reports confirm high rates of engraftment and promising survival outcomes after double UCB transplantation (23, 24, 29-33). Rates of sustained engraftment of % are reported after double UCBT, both after myeloablative and non-myeloablative conditioning regimens. The number of adult patients transplanted with UCBT has increased following the use of RIC regimen and double CB transplants. The Minnesota group has evaluated the efficacy of UCB in the setting of a non-myeloablative regimen consisting of fludarabine (200 mg/m 2 ), cyclophosphamide (50 mg/kg) and a single fraction (200 cgy) of total body irradiation with cyclosporin and mycophenolate mofetil for post-transplantation immunoprophylaxis (23). The target cell dose for the UCB graft was 3x10 7 nucleated cells/kg, resulting in the selection of a second partially HLA-matched UCB unit in 85%. Data reported to the Center for International Blood and Marrow Transplant Research (CIBMTR) suggest that the numbers of double UCB transplantations being performed are increasing and that these now account for approximately 80% of UCB transplantations for adults in the United States. The decision to infuse 2 UCB units varies between institutions (34-36). Of the 947 cord blood transplants performed in Italy from 2000 to 2012, 908 were single and 39 were double (GITMO). In Europe, 9300 cord blood transplants were performed from 1988 to 2012, of which 1900 were derived from double cord blood units (Eurocord). These data underline the fact that, in Italy, 4% of cord blood transplants were performed using double units, while in Europe this procedure has become more established, accounting for 20% of all cord blood transplants (Figure 1). Remarkably, sustained hematopoiesis is usually derived from a single donor, and one of the CBUs disappears or does not engraft at all. In most patients, single-donor chimerism is generally documented within three months post transplantation, but may occur even earlier (23). The mechanism of predominance of a particular unit, however, has not yet been clarified. Several explanations have been brought forward, including immunological rejection and insufficient cell viability. Some authors have shown that unit predominance may also be

4 116 R. Angarano, et al. Europe CB transplantation CB tot = 9300 CB double = 1900 (20%) Italy CB transplantation CB tot = 947 CB single = 908 CB double = 39 (4%) Figure 1 Single and double cord blood (CB) transplantations carried out in Europe and in Italy. influenced by post-thaw viability (37), length of time between the infusion of the 2 UCB units (38), and ex vivo expansion (39, 40). Ramirez et al. suggest that, following ducbt with 2 unmanipulated units of similar quality (as measured by viability) infused within a short interval ( 30 min), the main determinants of UCB predominance are CD3+ cell dose and, in the setting of nonmyeloablative conditioning, HLAmatching (41). Also T cells can mediate predominance after ducbt as described in smaller numbers of patients (42-44). Gutman et al. showed that, after ducbt, a subset of CD8+ memory T cells derived from the engrafting unit rapidly emerged after transplant and produced interferon-γ in response to the non-predominant UCB unit (47). Many factors, related to the UCB unit and environment, play a role in longterm unit predominance after ducbt. Despite evidence suggesting an immunologically mediated mechanism underlying unit predominance, there are several questions that remain to be answered (41). Incidence and severity of GVHD, relapse rate and TRM, both after standard myeloablative or reduced intensity regimen, in double UCB transplantations versus single unit are matters of debate. Reports from a single institution suggest a higher risk of grade 2 acute GVHD and lower risk of relapse after double UCB transplantation in patients with acute leukemia (45) (Table 1) (15, 44-48). A potential mechanism for the observed increase in acutegvhd after double UCBT may be the higher cell dose and the fact that the increased risk of acute GVHD was predominantly limited to the skin (44). While there was more stage III skin acute GVHD after double UCBT, incidences of liver and gastrointestinal tract acute GVHD were similar. Interestingly, the grade II acutegvhdobserved in double UCBT in the MacMillan study was associated

5 Double cord blood transplantation 117 with lower TRM (44) (Table 1). While the mechanism for this is unclear, it is possible that lower TRM is principally related to the higher cell dose associated with double UCBT with an effect that is independent of acute GVHD. So far, there have been several reports from single centers (30-33), and one multicenter phase II clinical trial (45), that demonstrate the potential effectiveness of double UCB transplantation for adults with hematologic malignancies. Rocha and colleagues report lower risk of relapse after double UCB compared with single UCB transplantations for patients with acute leukemia in first but not in second CR (46) (Table 1). Double-unit UCB transplants after myeloablative conditioning regimenshave been linked with lower relapse rates than other donor types, though they are also associated with longer time to hematopoietic engraftment and subsequent higher rates of NRM compared to reduced RIC. In a recent study, members of the Eurocord network showed that the use of double-unit UCB transplants was associated also with an improved leukemia-free survival compared with single UCB transplants in the acute leukemia setting of patients using reduced intensity conditioning regimen (47) (Table 1). Also Verneris and colleagues report lower relapse risks in patients with acute myeloid leukemia or acute lymphoblastic leukemia who received transplants in first or second CR after double UCB compared with single UCB transplantation (45). However, neither report (45, 46, 49) demonstrated differences in overall or leukemia-free survival (Table 1). These data suggest that the use of 2 UCB units is associated with an enhanced GVL effect. Although recipients of 2 UCB units received significantly more T cells than single-unit patients, neither T-cell dose nor age was associated with grade II- IV acute GVHD. Some authors speculate that increased alloreactivity may TABLE 1 Relapse rates and leukemia-free survival after double umbilical cord blood (UCB) compared with single UCB transplantation. Single cord blood unit Double cord blood unit References agvhd II-IV MacMillan et al., 2009 (44) GVL effect Verneris et al., 2009 (45) Incidence of relapse at 2 years (CR1-CR2) Verneris et al., 2009 (45) Saccardi et al., 2012 (15); Rocha, 2010 (46) (CR1 only); Rocha, 2013 (47) = Scaradavou, 2013 (48) 2g-LFS in AL (RIC in CR1) Saccardi et al., 2012 (15) TRM = = Scaradavou, 2013 (48) MacMillan et al., 2009 (44) (at 1 year) agvhd, graft-versus-host disease; GVL,graft-versus-leukemia; CR, complete response; LFS, leukemia-free survival; AL, acute leukemia; RIC, reduced intensity conditioning; TRM, transplant-related mortality.

6 118 R. Angarano, et al. be induced by the graft-graft interaction between the 2 UCB units, and this may be responsible for the apparent reduction in the risk of relapse following double UCB transplantation. However, the mechanism of this and the effect or cell population remain unclear (45). These results may suggest that double UCB transplant results in better disease control than either single-unit UCB transplant or more conventional sources (i.e. BM or PB from unrelated donors). However, prospective clinical trials are required to confirm this. In contrast to what has been reported by others, Scaradavou et al. did not observe significant differences in relapse risks or overall mortality after single and double UCB transplantations (Table 1), while mortality risks were higher for patients who received transplants in relapse and second or third CR compared to those who received transplants in first remission, showing that the most important determinant of survival after transplantation of double or single UCB units was disease status at transplantation (48). The risk of TRM was associated with the overall degree of HLA disparity. Only an estimated 25% of adults will be able to find a suitable single UCB unit, and studies on the safety and effectiveness of double UCB unit transplantations are underway to address the obstacle presented by cell-dose. In the absence of a randomized clinical trial, when an 8/8 HLA-matched unrelated adult donor is not available and when a transplant is needed urgently, possible options are the use of 4-6/6 HLA matched unrelated UCB or the infusion of 2 partially HLA-matched UCB units that could effectively create an adequately dosed graft for patients lacking access to a single UCB unit containing TNC/ kg or more (50). Having established that UCB is a suitable alternative source, and that transplantation of 2 UCB units is a safe and efficient way to extend transplantation to the many adults with leukemia who lack a single UCB with an adequate TNC, early referral for transplantation will likely improve survival. References 1. Gratwohl A. Can we afford to continue hematopoietic stem cell transplantation? Drugs Cell Ther Hematol 2013; 2: Knudtzon S. In vitro growth of granulocytic colonies from circulating cells in human cord blood. Blood 1974; 43: Leary AG, Ogawa M. Blast cell colony assay for umbilical cord blood and adult bone marrow progenitors. Blood 1987; 69: Broxmeyer HE, Douglas GW, Hangoc G, et al. Human umbilical cord blood as a potential source of transplantable hematopoietic stem/progenitor cells. Proc Natl Acad Sci USA 1989; 86: Gluckman E, Broxmeyer HA, Auerbach AD, et al. Hematopoietic reconstitution in a patient with Fanconi s anemia by means of umbilical-cord blood from an HLA-identical sibling. N Engl J Med 1989; 321: Rocha V, Labopin M, Sanz G, et al. Transplants of umbilical-cord blood or bone marrow from unrelated donors in adults with acute leukemia. N Engl J Med 2004; 351: Rocha V, Cornish J, Sievers EL, et al. Comparison of outcomes of unrelated bone marrow and umbilical cord blood transplants in children withacute leukemia. Blood 2001; 97: Wagner JE, Barker JN, DeFor TE, et al. Transplantation of unrelated donor um-

7 Double cord blood transplantation 119 bilical cord blood in 102 patients with malignant and non malignant diseases: influence of CD34 cell dose and HLA disparity on treatment-related mortality and survival. Blood 2002; 100: Laughlin MJ, Eapen M, Rubinstein P, et al. Outcomes after transplantation of cord blood or bone marrow from unrelated donors in adults with leukemia. N Engl J Med 2004; 351: Laughlin MJ, Barker J, Bambach B, et al. Hematopoietic engraftment and survival in adult recipients of umbilical-cord blood from unrelated donors. N Engl J Med 2001; 344: MacMillan ML, Weisdorf DJ, Brunstein CG, et al. Acute graft-versus-host disease after unrelated donor umbilical cord blood transplantation: analysis of risk factors. Blood 2009; 113: Rocha V, Wagner JE Jr., Sobocinski KA, et al. Graft-versus-host disease in children who have received a cordblood or bone marrow transplant from an HLA-identical sibling. Eurocord and International Bone Marrow Transplant Registry Working Committee on Alternative Donor and Stem Cell Sources. N Engl J Med 2000; 342: Eapen M, Rubinstein P, Zhang MJ, et al. Outcomes of transplantation of unrelated donor umbilical cord blood and bone marrow in children with acute leukaemia: a comparison study. Lancet 2007; 369: Locatelli F, Rocha V, Chastang C, et al. Factors associated with outcome after cord blood transplantation in children with acute leukemia. Eurocord - Cord Blood Transplant Group. Blood 1999; 93: Saccardi R, Ruggeri A, Labopin M, et al. Determining timing of late engraftment and graft failure following single cord, unrelated transplantation: an analysis of the Eurocord Registry (EBMT Annual meeting). Abstract Rocha V, Cornish J, Sievers EL, et al. Comparison of outcomes of unrelated bone marrow and umbilical cord blood transplants in children with acute leukaemia. Blood 2001; 97: Niehues T, Rocha V, Filipovich AH, et al. Factors affecting lymphocyte subset reconstitution after either related or unrelated cord blood transplantation in children-a Eurocord analysis. Br J Haematol 2001; 114: Komanduri KV, St John LS, De Lima M, et al. Delayed immune reconstitution after cord blood transplantation is characterized by impaired thymopoiesis and late memory T-cell skewing. Blood 2007; 110: Rocha V, Gluckman E; Eurocord-Netcord registry and European Blood and Marrow Transplant group. Improving outcomes of cord bloodtransplantation: HLA matching, celldose and other graft- and transplantation-related factors. Br J Haematol 2009; 147: Frassoni F, Gualandi F, Podestà M, et al. Direct intrabone transplant of unrelated cord-blood cells in acute leukaemia: a phase I/II study. Lancet Oncol 2008; 9: Delaney C, Varnum-Finney B, Aoyama K, et al. Dose-dependent effects of the Notch ligand Delta1 on ex vivo differentiation and in vivo marrow repopulating ability of cord blood cells. Blood 2005; 106: de Lima M, McMannis J, Gee A, et al. Transplantation of ex vivo expanded cord blood cells using the copper chelator tetraethylenepentamine: a phase I/II clinical trial. Bone Marrow Transplant 2008; 41: Brunstein CG, Barker JN, Weisdorf DJ, et al. Umbilical cord blood transplantation after nonmyeloablative conditioning: impact on transplantation outcomes in 110 adults with hematologic disease. Blood 2007; 110: Barker JN, Weisdorf DJ, DeFor TE, et al. Rapid and complete donor chimerism in adult recipients of unrelated donor umbilical cord blood transplantation after reduced-intensity conditioning. Blood 2003; 102:

8 120 R. Angarano, et al. 25. Ballen K, Spitzer TR, Yeap BY, et al. Double unrelated reduced-intensity umbilical cord blood transplantation in adults. Biol Blood Marrow Transplant 2007; 13; Fernandes J, Rocha V, Robin M, et al. Second transplant with two unrelated cord blood units for early graft failure after haematopoietic stem cell transplantation. Br J Haematol 2007; 137: Bautista G, Cabrera JR, Regidor C, et al. Cord blood transplants supported by co-infusion of mobilized hematopoietic stem cells from a third-party donor. Bone Marrow Transplant 2009; 43: MacMillan ML, Blazar BR, DeFor TE, Wagner JE. Transplantation of ex-vivo culture-expanded parental haploidentical mesenchymal stem cells to promote engraftment in pediatric recipients of unrelated donor umbilical cord blood: results of a phase I-II clinical trial. Bone Marrow Transplant 2009; 43: Barker JN, Weisdorf DJ, DeFor TE, et al. Transplantation of 2 partially HLAmatched umbilical cord blood units to enhance engraftment in adults with hematologic malignancy. Blood 2005; 105: Cutler C, Stevenson K, Kim HT, et al. Double umbilicalcord blood transplantation with reducedintensity conditioning and sirolimus-based GVHD prophylaxis. Bone Marrow Transplant 2011; 46: Avery S, Shi W, Lubin M, et al. Influence of infusedcell dose and HLA-match on engraftmentafter double unit cord blood allografts. Blood 2011; 117: Ponce DM, Zheng J, Gonzales AM, et al. Reducedlate mortality risk contributes to similar survivalafter double-unit cord blood transplant comparedwith related and unrelated donorhematopoietic stem cell transplant. Biol Blood Marrow Transplant 2011; 17: Brunstein CG, Gutman JA, Weisdorf DJ, et al. Allogeneic hematopoietic cell transplantation forhematologic malignancy: relative risks and benefitsof double umbilical cord blood. Blood 2010; 116: Delaney C, Gutman JA, Appelbaum FR. Cordblood transplantation for haematoloigc malignancies: conditioning regimens, double cord bloodtransplants and infectious complications. Br J Haematol 2009; 147: Barker JN, Byam C, Scaradavou A. How I treat: the selection and acquisition of unrelated cordblood grafts. Blood 2011; 117: Gluckman E, Rocha V, Arcese W, et al. Factors bassociated with outcomes of unrelated cord bloodtransplant: guidelines for donor choice. Exp Hematol 2004; 32: Scaradavou A, Smith KM, Hawke R, et al. Cord blood units with low CD34+ cell viability have alow probability of engraftment after double unit transplantation. Biol Blood Marrow Transplant 2010; 16: Haspel RL, Kao G, Yeap BY, et al. Preinfusion variables predict the predominant unit in thesetting of reduced-intensity double cord blood transplantation. Bone Marrow Transplant 2008; 41: Delaney C, Heimfeld S, Brashem-Stein C, et al. Notch-mediated expansion of human cord bloodprogenitor cells capable of rapid myeloid reconstitution. Nat Med 2010;16: De Lima M, Robinson S, McMannis J, et al. Mesenchymal stem cell based cord blood expansion leads to rapid engraftment of platelets and neutrophils. Blood 2010; 116: Ramirez P, Wagner JE, DeFor TE, et al. Factors predicting single-unit predominance after double umbilical cord blood transplantation. Bone Marrow Transplant 2012; 47: Gutman JA, Turtle CJ, Manley TJ, et al. Single-unit dominance after double-unit umbilical cordblood transplantation coincides with a specific CD8+ T-cell response against the nonengraftedunit. Blood 2010;115:

9 Double cord blood transplantation Eldjerou LK, Chaudhury S, Baisre-de Leon A, et al. An in vivo model of double-unit cord bloodtransplantation that correlates with clinical engraftment. Blood 2010; 116: MacMillan ML, Weisdorf DJ, Brunstein CG, et al. Acute graft-versus-host disease after unrelated donor umbilical cord blood transplantation: analysis of risk factors. Blood 2009; 113: Verneris MR, Brunstein CG, Barker JN, et al. Relapse risk after umbilical cord blood transplantation: enhanced graft-versus-leukemia effect in recipients of two units. Blood 2009; 114: Rocha V, Labopin M, Mohty M, et al. Outcomes after double unit unrelated cord blood transplantation (UCBT) compared with single UCBT in adults with acute leukemia in remission. A Euorcordand ALWP Collaboration study [abstract]. Blood (ASH Annual Meeting Abstracts) 2010; 116: Abstract Rocha V, Labopin M, Ruggeri A, et al. Comparison between single and double cord blood transplantations in adults with acute leukaemia receiving reduced intensity conditioning regimen (EBMT Annual meeting). Abstract 2013; O Scaradavou A, Brunstein CG, Eapen M, et al. Double unit grafts successfully extend the application of umbilical cord blood transplantation in adults with acute leukemia. Blood 2013; 121: Brunstein CG, Fuchs EJ, Carter SL, et al. Alternative donor transplantation: results of parallel phase II trials using HLAmismatched related bone marrow or unrelated umbilical cord blood grafts. Blood 2011; 118: Eapen M, Rocha V, Sanz G, et al. Effect of graft source on unrelated donor haemopoietic stem-cell transplantation in adults with acute leukaemia: a retrospective analysis. Lancet Oncol 2010; 11:

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