Sibling Donor Cord Blood Transplantation for Thalassemia Major: Experience of the Sibling Donor Cord Blood Program

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1 Sibling Donor Cord Blood Transplantation for Thalassemia Major: Experience of the Sibling Donor Cord Blood Program MARK C. WALTERS, LYNN QUIROLO, ELIZABETH T. TRACHTENBERG, SANDIE EDWARDS, LISA HALE, JOANNA LEE, JOI MORTON-WILEY, KEITH QUIROLO, SHANDA ROBERTSON, JULIE SABA, AND BERT LUBIN Children s Hospital & Research Center at Oakland, Oakland, California 94609, USA ABSTRACT: The Sibling Donor Cord Blood (SDCB) Program was initiated in 1998 as a resource to collect, characterize, and release cord blood units (CBUs) from families affected by malignant and nonmalignant disorders for transplantation. Families in the United States were recruited by telephone after referrals by community and academic physicians. Collection kits were mailed to prospective participants and family members were instructed about CBU procurement from community hospitals and shipping to a central laboratory. Data about the infant s delivery and CBU harvest, CBU processing, prethaw characteristics, sterility, and human leukocyte antigen (HLA) typing were collected. Standard outcome data were collected after CBU release for transplantation. Descriptive analyses of CBU collections, processing, release, and transplantation outcomes were performed. Currently, 1617 CBU collections have been processed from families with thalassemia (6%), sickle cell disease (28%), malignant disorders (49%), and other rare hematological disorders (17%). Thirty-two of 96 donor recipient pairs with thalassemia major were HLA identical and 14 have received cord blood transplantation, either alone or in combination with bone marrow or peripheral blood progenitor cells (N = 4) from the same donor. Eleven of the 14 survive free of thalassemia after transplantation. These preliminary results confirm the feasibility and utility of remote-site sibling donor cord blood collection and subsequent transplantation for hematological disorders, with a very high rate of usage from a cord blood bank dedicated to performing these unique collections. It was concluded that cord blood transplantation from sibling donors represents a suitable alternative to bone marrow transplantation. KEYWORDS: transplantation; thalassemia; human leukocyte antigen; cord blood INTRODUCTION Since the first successful report of transplantation for thalassemia major two decades ago, significant advances in the optimal selection of individuals who might Address for correspondence: Mark C. Walters, Children s Hospital & Research Center at Oakland, nd St., Oakland, CA Voice: ; fax: Ann. N.Y. Acad. Sci. 1054: (2005) New York Academy of Sciences. doi: /annals

2 WALTERS et al.: SIBLING DONOR CORD BLOOD TRANSPLANTATION 207 benefit from this intervention, coupled with advances in supportive care, have generated better outcomes after hematopoietic cell transplantation. 1 4 Currently, a focus of research is to broaden the availability of transplantation by using hematopoietic stem cell sources other than bone marrow from human leukocyte antigen (HLA) identical sibling donors. 5,6 To this end, we have established and expanded a Sibling Donor Cord Blood (SCDB) Bank that was created to benefit families with thalassemia major and other disorders treatable by transplantation. 7,8 As a public resource for families expecting a full sibling of a child with a hematological, immunological, or oncological disorder, more than 1600 cord blood units (CBUs) have been collected, characterized, and cryopreserved by the Sibling Donor Cord Blood Program in Oakland, California. In this report, we describe the program, summarize its activity to date, and report the preliminary outcome of transplantation for thalassemia when CBUs released by our cord blood bank were used. Cord blood transplantation offers potential benefits in its immediate availability, in a reduced risk of graft-versus-host disease (GVHD) compared with other stem cell sources, particularly among those with genetic disorders for whom the graft-versushost reaction has no benefit, and in the elimination of risk and discomfort to donors. 9,10 Its chief disadvantages are a limiting number of hematopoietic progenitor cells and delayed time to engraftment, which together are associated with a risk of nonengraftment and accompanying opportunistic infections. However, the tempo of immune reconstitution is similar to and even more rapid than after transplantation from other hematopoietic cell sources. 11 Preliminary results of sibling CB transplantation for children with severe hemoglobinopathies are particularly encouraging and indicate that this treatment option may prove important in the future. 12 To create a public resource for families and to support future investigations of CB transplantation, we established a CB banking resource in Although initial CB transplantation experience involved directed sibling donations, no standardized resource for sibling CB banking had been developed before this effort, and most reports of umbilical cord blood (UCB) banking focused on unrelated donors. 13,14 In particular, CBUs were rarely available when procurement and processing from remote, community-based hospitals was a requirement for banking. Here, we report the updated experience of the SDCB Program and also speculate about when a CBU might be chosen for transplantation in lieu of marrow- or granulocyte-colony stimulating factor (G-CSF) mobilized peripheral blood stem cells from a sibling donor. RESULTS The collection, characterization, and storage of CBUs was performed initially at no cost to participating families, but currently, in response to the growth of the program and its service population, it is performed for a nominal fee to families affected by oncological disorders, and free of charge to families with hemoglobinopathies. The value of the program has been validated in part by the sustained referral patterns and by the increased use of CBUs banked by this program for use in transplantation therapy. The growth of the program stemmed primarily from outreach efforts to inform the professional and lay public about this unique resource. These included the publication of a periodical newsletter, updated Web site, and dissemination of information about the program and transplant outcomes at professional and scientific meetings.

3 208 ANNALS NEW YORK ACADEMY OF SCIENCES FIGURE 1. Sibling donor CB collections by disease category. The SDCB Program has banked a total of 1617 CB collections since its inception. The demographics by disease category are depicted in this pie chart, with each category designated by filled segments. Most collections occurred for the indication of malignant disorders; however, collections in families affected by hemoglobinopathies accounted for many of the cases. Since the program s inception in 1998, the program has enrolled 1751 families and banked 1617 CBU collections. The enrollments categorized by disease are shown in FIGURE 1. While 48% of the collections occurred in families affected by hematological malignancies, 28% of collections were performed for sickle cell disease families and 6% for thalassemia families. Families affected by metabolic storage disease, immunodeficiency diseases, and other hematological disorders accounted for 15% of the total. Thus, our outreach efforts to promote enrollment in families with hemoglobinopathies have been very successful, and compared with the national transplantation rates for these disorders, there is a significant overrepresentation of hemoglobinopathy families in the SDCB Program Bank. The annual case collection enrollment is depicted in FIGURE 2 and includes 1751 families enrolled since the inception of the program. As shown, the distribution of cases enrolled has not varied significantly from year to year. The plateau observed in case enrollment is the consequence of new policies that were instituted to optimize the use of CBUs and to focus on collections in families with hereditary hematological disorders. The characteristics of the CB units are summarized in TABLE 1. After processing, the median total nucleated cell count was 9.4 ± and the median CD 34 + cell content was 3.7 ± The rate of bacterial contamination as measured by aerobic and anaerobic culture was 3.3%. Collections with volumes less than 20 ml were not processed, and these low-volume collections accounted for 4.4% of the CBUs received for processing. Thus, most CBUs underwent processing and cryopreservation, were free of bacterial contamination, and had a cellular content that was projected to be adequate for engraftment, based on the weight of the prospective recipient reported to the SDCB Program at collection. To screen sibling CB collections for transplantation suitability, Class I HLA-A, HLA-B, and class II HLA-DRB1 DNA typing were performed at an intermediate level of resolution. Since having a full sibling was a requirement for enrollment,

4 WALTERS et al.: SIBLING DONOR CORD BLOOD TRANSPLANTATION 209 FIGURE 2. Annual enrollment in the SDCB Program. The number of new cases enrolled annually in the SDCB Program is presented from 1998 to The annual enrollment is also characterized by disease category, as indicated by hatched segments in the columns representing cases. The cumulative enrollment over this period was 1751 cases. TABLE 1. Characteristics of cord blood units processed by the SDCB Program Mean SD Range Volume (w/35 ml anticoagulant) Total nucleated cells (TNC) Total mononuclear cells (MNC) CD34 + /collection CFU/collection 10 6, n = Recovery (%), n = NOTE: Failed sterility test: 54 out of 1635 units. Number of CB released: total of 52 units. TNC, MNC, CD34 +, and CFU values are postprocessing data. high-resolution (allelic) analysis was used rarely, and only to resolve ambiguities when they occurred in the donor screening. If there was one or fewer antigen mismatch at HLA-A and B, the DRB1 locus was analyzed. Using this strategy, we observed that only 33% of cases required class II analysis, as the objective of the CBU banking program is to identify HLA-identical donor host pairs. To date, 1114 of the 1617 CBUs banked have been analyzed by HLA typing. Overall, 259 of the CBUs were HLA identical to the prospective recipient (23%),

5 210 ANNALS NEW YORK ACADEMY OF SCIENCES and 16 and 87 CBUs were mismatched for one and two HLA antigens, respectively. Ninety-four collections for thalassemia major were analyzed (α-thalassemia, N = 6 and β-thalassemia, N = 88) by HLA typing. Of these, 32 (34%) donor recipient pairs were HLA identical. Three hundred eighty-nine CBUs were collected from families affected by sickle cell disease. The observed frequency of having an HLA-identical CBU was 23% (120 of 389) among the sickle cell disease families, and the lower frequency compared to thalassemia might reflect a higher degree of HLA heterogeneity among African-Americans compared with non-african thalassemia populations. There was a high rate of CBU use for transplantation by families affected by thalassemia major. Of 102 thalassemia collections performed, 15 have been released, and 14 CBUs were used for transplantation (14% of CBUs collected). The rate of CBU use for transplantation among thalassemia families with HLA-identical siblings was 44% (14 of 32). This compares with a usage rate of 9% in sickle cell disease (8 of 89 HLA-identical pairs), 8.5% in acute myelogenous leukemia (7 of 82 collections), and 1.4% in acute lymphoblastic leukemia (9 of 636 collections). Thus, it appears that thalassemia families that participate in the SDCB Program are very motivated to proceed to transplantation if a suitable CBU is identified. Overall, the rate of CBU use in related donors is somewhat higher than the rate observed by unrelated donor banks, as expected. 15,16 To date, 47 patients have proceeded to transplantation, supported by the sibling donor CBU either alone (N = 37) or in combination with marrow or peripheral blood stem cells (N = 10) from the same sibling donor as the source of allogeneic hematopoietic cells. The median follow-up is 12.4 months with a range of months. These patients had thalassemia (N = 14), sickle cell disease (N = 8), acute leukemia (N = 16), myelodysplastic syndrome (N = 1), or other nonmalignant hematological disorders (N = 8). All but five received HLA-identical sibling allografts, and four patients received haploidentical allografts mismatched at two HLA loci. Thirty-eight of 47 patients survive after transplantation, 36 free of the underlying disease. The median time to absolute neutrophil count (ANC) of more than 500 and platelet count of more than 20,000/mm 3 was 23 and 45 days, respectively. Graft failure associated with disease relapse was observed in two patients with acute leukemia and in one patient with thalassemia, and one additional patient received a CB boost to treat graft rejection after a nonmyeloablative marrow transplantation, and the CB infusion was unsuccessful in reversing the rejection. Six patients died of relapsed leukemia, one patient with sickle cell anemia died of intractable seizures approximately 100 days after transplantation, and two more patients with hemoglobinopathies died of pulmonary toxicity after CB transplantation. In total, 18 of 22 patients with sickle cell disease or thalassemia survive event-free after transplantation, which includes 12 of 14 patients with thalassemia major. One patient with thalassemia had disease recurrence after transplantation. The Kaplan Meier probability of survival after sibling donor CB transplantation is 75% among 44 patients for whom there is at least 6 months of follow-up (FIG. 3). The indications for transplantation are shown in the figure, and include five patients who received HLA-mismatched CB grafts for advanced disease. The transplants were performed in 31 U.S. transplantation centers, and patients were prepared with a variety of conditioning regimens that were tailored to the underlying disease. Similarly, therapy to prevent GVHD varied from center to center. There were no deaths related to GVHD.

6 WALTERS et al.: SIBLING DONOR CORD BLOOD TRANSPLANTATION 211 FIGURE 3. Survival and event-free survival after sibling donor CB transplantation. The Kaplan Meier probabilities of survival and event-free survival after sibling donor CB transplantation is shown. Time after transplantation in months is indicated in the x axis. Events were defined as death, graft rejection, or relapse, and patients were censored at the time of an event. The indications for transplantation are shown.

7 212 ANNALS NEW YORK ACADEMY OF SCIENCES DISCUSSION Despite the challenge of remote-site CB collections caused by the unpredictable timing of birth and linguistic and cultural barriers, this experience demonstrates that sibling CBU collection in the United States can be accomplished in a closed collection system, with uniform standardized procedures and rigorous quality systems. Approximately 90% of units processed by the program had characteristics that made them acceptable for allogeneic CB transplantation. The transplantation outcomes reported here strongly suggest that sibling CBUs will continue to be used, especially in children with thalassemia major and other hereditary disorders. It is notable that we have observed this usage pattern even though, in most instances, bone marrow harvesting from the same sibling donor was also available. Use of CBUs by children with malignant diseases was lower, but this reflects the fact that more than 95% of these children were receiving either primary induction therapy or were in a first remission at the time of sibling CB banking. While a longer period of follow-up will be necessary to determine the true rate of sibling CB use for malignant disorders, our preliminary experience suggests that more families with hereditary hematological disorders are motivated to proceed immediately to sibling CB transplantation. This preliminary experience also indicates that, like marrow, CB might also be considered as an acceptable source of allogeneic cells for HLA-identical sibling hematopoietic cell transplantation. The principal advantage in the setting of hereditary disorders such as thalassemia major has to do with a lowered risk of GVHD after transplantation, a complication that has no apparent beneficial effect for these disorders, but rather is a leading cause of morbidity and mortality after transplantation. 1 This benefit, however, must be weighed carefully against the potential for delayed engraftment and graft rejection, which also can contribute to the toxicity of transplantation. 12 This risk has been countered successfully by the administration of immunosuppressive therapy before transplantation and by the supplementation with sibling donor marrow when the cellular content of the CBU is judged insufficient to guarantee engraftment. This strategy has proved quite successful as demonstrated by the excellent outcomes after SDCB transplantation reported here. Together with a very high rate of use and enthusiastic participation by families who could benefit from this program, we believe that banking sibling CBUs represents an important public resource, which warrants ongoing support to expand and maintain this service. In addition, it is possible and even likely that this bank will act as a core resource to support ongoing and future research aimed at studying the capacity of UCB stem cells to repair preexisting organ damage after transplantation and to study novel gene transfer vectors whose transduction rates might be optimized in UCB stem cells. REFERENCES 1. GAZIEV, J. & G. LUCARELLI Stem cell transplantation for thalassaemia. Reprod. Biomed. Online 10: LUCARELLI, G., M. GALIMBERTI, P. POLCHI, et al Bone marrow transplantation in patients with thalassemia. N. Engl. J. Med. 322: SODANI, P., D. GAZIEV, P. POLCHI, et al New approach for bone marrow transplantation in patients with class 3 thalassemia aged younger than 17 years. Blood 104:

8 WALTERS et al.: SIBLING DONOR CORD BLOOD TRANSPLANTATION THOMAS, E.D., C.D. BUCKNER, J.E. SANDERS, et al Marrow transplantation for thalassaemia. Lancet 2: GAZIEV, D., M. GALIMBERTI, G. LUCARELLI, et al Bone marrow transplantation from alternative donors for thalassemia: HLA-phenotypically identical relative and HLA-nonidentical sibling or parent transplants. Bone Marrow Transplant. 25: LA NASA, G., C. GIARDINI, F. ARGIOLU, et al Unrelated donor bone marrow transplantation for thalassemia: the effect of extended haplotypes. Blood 99: REED, W., R. SMITH, F. DEKOVIC, et al Comprehensive banking of sibling donor cord blood for children with malignant and nonmalignant disease. Blood 101: REED, W., M. WALTERS & B.H. LUBIN Collection of sibling donor cord blood for children with thalassemia. J. Pediatr. Hematol. Oncol. 22: ROCHA, V, J.E. WAGNER, JR., K.A. SOBOCINSKI, et al Graft-versus-host disease in children who have received a cord-blood or bone marrow transplant from an HLAidentical sibling. Eurocord and International Bone Marrow Transplant Registry Working Committee on Alternative Donor and Stem Cell Sources. N. Engl. J. Med. 342: BARKER, J.N. & J.E. WAGNER Umbilical cord blood transplantation: current practice and future innovations. Crit. Rev. Oncol. Hematol. 48: TALVENSAARI, K., E. CLAVE, C. DOUAY, et al A broad T-cell repertoire diversity and an efficient thymic function indicate a favorable long-term immune reconstitution after cord blood stem cell transplantation. Blood 99: LOCATELLI, F., V. ROCHA, R.W. REED, et al Related umbilical cord blood transplantation in patients with thalassemia and sickle cell disease. Blood 101: COHEN, Y., D. KREISER, M. MAYOROV & A. NAGLER Unrelated and related cord blood banking and hematopoietic graft engineering. Cell Tissue Bank 4: RUBINSTEIN, P., C. CARRIER, A. SCARADAVOU, et al Outcomes among 562 recipients of placental-blood transplants from unrelated donors. N. Engl. J. Med. 339: KOGLER, G., T. SOMVILLE, G.U. GOBEL, et al Haematopoietic transplant potential of unrelated and related cord blood: the first six years of the EUROCORD/NET- CORD Bank Germany. Klin. Padiatr. 211: RUBINSTEIN, P., J.W. ADAMSON & C. STEVENS The Placental/Umbilical Cord Blood Program of the New York Blood Center. A progress report. Ann. N.Y. Acad. Sci. 872: ; discussion

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