UMBILICAL-CORD BLOOD TRANSPLANTATION FOR THE TREATMENT OF CANCER

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1 UMBILICAL-CORD BLOOD TRANSPLANTATION FOR THE TREATMENT OF CANCER Juliet N. Barker* and John E. Wagner Haematopoietic stem-cell transplantation is used to treat many haematological cancers, but is limited by the lack of suitable bone-marrow donors, the risk of graft-versus-host disease (GVHD) and slow immune reconstitution. Umbilical-cord blood is an alternative source of haematopoietic stem cells that has recently been tested in both child and adult cancer patients. These studies have identified several advantages to umbilical-cord cell transplantation, including a lower incidence of GVHD. Umbilical-cord blood is therefore a promising alternative to bone-marrow-derived stem cells. AUTOLOGOUS TISSUE Haematopoietic stem cells that are derived from the patient. ALLOGENEIC TISSUE Haematopoietic stem cells that are from an antigenically distinct individual of the same species from a sibling or unrelated donor. *Department of Medicine and Department of Pediatrics, Blood and Marrow Transplant Program of the University of Minnesota School of Medicine, 420 Delaware Street, S.E., Minneapolis, Minnesota 55455, USA. Correspondence to J.N.B. doi: /nrc1125 Haematopoietic stem-cell transplantation is the standard therapy for many cancers that originate in the blood and bone marrow. This transplantation procedure involves exposure of the patient to chemotherapy or chemoradiation to kill cancer cells, followed by infusion of haematopoietic stem cells to reconstitute the patient s bone marrow and immune system (FIG. 1). Either AUTOLOGOUS haematopoietic stem cells (collected from the patient before treatment) or ALLOGENEIC haematopoietic stem cells (collected from a related or unrelated donor) can be transplanted. Autologous transplantation is limited by stem-cell damage from previous cancer therapy and the potential contamination with malignant cells. Furthermore, as autologous transplantation is associated with only a minimal immune response against the tumour, the risk of relapse is significant. By contrast, allogeneic transplantation involves the infusion of healthy haematopoietic stem cells from a related or unrelated donor. In some cases, the reconstituted donor immune system can recognize and destroy the host s tumour a process that is known as the GRAFT-VERSUS-LEUKAEMIA (GVL) or graft-versus-malignancy effect. The GVL effect has been described in patients who have received bone-marrow transplants not only to treat haematological cancers, but also for other cancers such as renal-cell carcinoma. The widespread use of allogeneic haematopoietic stem-cell transplantation has, however, a number of important limitations. These include a shortage of available matched sibling or matched unrelated marrow donors, the length of the unrelated marrow search process (which averages 4 months), and the risk of developing GRAFT-VERSUS-HOST DISEASE (GVHD). Appropriate related or unrelated bone-marrow donors are restricted to those matched for specific MAJOR HISTOCOMPATIBILITY ANTIGENS. Human leukocyte antigen (HLA) matching is required to prevent the devastating immune complications of graft rejection, GVHD and slow or incomplete immune reconstitution, and consequent risk of lethal opportunistic infection (BOX 1). The chance of a patient s full sibling being HLA identical is one in four. With increasingly restricted family sizes, only 30% of patients have a sibling donor who is matched for five or six of the six HLA loci (BOX 1). Bone-marrow registries, which list more than 7 million volunteer donors worldwide, have been created to help patients find suitable bone-marrow donors. However, whereas Caucasian patients have good odds of finding a match through these registries, people of non-northern European descent, or others with rare HLA haplotypes, have a poor likelihood of finding a suitable donor. Also, the genetic heterogeneity 526 JULY 2003 VOLUME 3

2 GRAFT-VERSUS-LEUKAEMIA (GVL) EFFECT The ability of the immune cells that are derived from transplanted haematopoietic stem cells to recognize and destroy leukaemia cells. This partially accounts for the mechanism of action of allogeneic transplantation as treatment for leukaemia. The term has been broadened to graft-versus-malignancy, to acknowledge that this effect is seen in patients with nonleukaemic diseases, such as myeloma or lymphoma. Summary Allogeneic bone-marrow transplantation is the best treatment for patients with haematological cancers. This procedure, however, is limited by lack of suitable donors, as well as the complications of graft-versus-host disease (GVHD) and opportunistic infection. Umbilical-cord blood is an excellent source of haematopoietic stem cells. It has the advantages of speedy availability and reduced incidence of causing GVHD. This allows for transplantation of grafts with limited HLA disparity, and thereby extends the donor pool. The main determinants of successful umbilical-cord blood transplant are the number of cells that are available for transplantation and HLA matching. Cord blood transplantation has been validated as an alternative to bone-marrow transplantation for the treatment of leukaemia in children. A number of approaches are being developed to improve the efficacy of cord blood transplantation in adults, such as multiple-unit transplantation and reduced intensity of chemo-radiation therapy. GRAFT-VERSUS-HOST DISEASE (GVHD). A complication of allogeneic haematopoietic transplantation. It occurs when the immune system of the donor graft recognizes the tissues of the recipient (host) as foreign and attacks them. This can be lethal in its most severe form. that is present in some ethnic groups, such as African Americans, magnifies the problem of an inadequate pool of donors. Furthermore, efforts to improve transplant outcomes by improving HLA MATCHING via matching based on high-resolution typing of HLA Class I loci, or extended typing of loci beyond HLA-A, HLA-B and DRB1 can delay or eliminate the availability of suitable donors for many patients. Finally, even patients who receive bone marrow from an HLA-A, B, DRB1-matched bone-marrow donor still face the frequent complication of GVHD, delayed immune reconstitution and the risk of acquiring opportunistic infections. So, bone-marrow transplantation is still a high-risk procedure. There is a great need for an alternative source of stem cells that can be easily and rapidly obtained, does not require a complete HLA match and is less likely to induce severe GVHD. Transplant: Autologous OR Allogeneic HSC Transplant outcome: Age and fitness of patient Response of tumour to chemotherapy, radiotherapy and GVL effect (after allogeneic transplant only) Prophylaxis and treatment of: Infection GVHD (after allogeneic transplant only) Immunosuppression (for allogeneic transplant only) Chemotherapy Radiation Figure 1 Treatment regimen and factors influencing the outcome of haematopoietic stem-cell transplantation. Patients who receive stem-cell transplants for haematological malignancies are first treated by a regimen of chemotherapy or chemoradiation for a period of up to 7 days (starting at day 7 on the therapeutic timeline). They then receive either autologous or allogeneic haematopoietic stem cells (day 0 on the timeline). Autologous transplantation involves collection of the patient s own haematopoietic stem cells, which are reinfused after high-dose chemotherapy or chemoradiation. In allogeneic transplantation, related or unrelated donor haematopoietic stem cells are infused after either a high-dose or reducedintensity preparative regimen. Patients also receive immunosuppressive drugs to prevent rejection of the transplanted cells. The main determinants of outcome include the susceptibility of the patient s cancer to the chemoradiation therapy, the induction of a graft-versus-leukaemia (GVL) effect by the transplanted immune system (allogeneic transplant only), and the patient s level of fitness (determined by age, previous cancer therapy and previous infections). The nature of the preparative regimen and the source of stem cells can also affect outcome. Other important variables in allogeneic transplant include the type of immunosuppressive drugs given to the patient, the methods of prophylaxis, and development of graft-versus-host disease, as well as opportunistic infections. Umbilical-cord blood Cord blood, which is collected from the umbilical cord and placenta of healthy newborns, is an alternative source of haematopoietic stem cells. It is usually collected after the delivery of the placenta, although collection during the third stage of labour is also possible. Compared with adult peripheral blood or bone marrow, cord blood contains a greater proportion of highly proliferative haematopoietic progenitor cells 1 8. Although the exact reason that these progenitors are present in the cord blood of newborns is unknown, it could relate to the placental production of growth factors, such as granulocyte colony-stimulating factor (G-CSF), which is known to mobilize haematopoietic stem cells. The use of cord blood as a source of haematopoietic stem cells for transplantation was proposed by Hal Broxmeyer and colleagues in In 1988, cord blood was first transplanted from a related donor to treat a patient with Fanconi anaemia 9, and the first cord blood transplant from an unrelated donor was performed in The demonstration that the bone marrow and immune systems of paediatric patients could be reconstituted after MYELOABLATIVE chemoradiation led to the emergence of cord blood as an alternative stem-cell source from both related 10,11 and unrelated donors. Umbilical-cord cells can be collected without risk to the donor, cryopreserved, stored for long periods of time without damage and easily shipped to any transplant centre. The first cord blood bank was created in Broxmeyer s laboratory at the Indiana University School of Medicine 19, and reports of the NATURE REVIEWS CANCER VOLUME 3 JULY

3 Box 1 Human leukocyte antigen (HLA) typing Immune complications after allogeneic transplantation are caused by differences in histocompatibility antigens between donor and recipient. The most important of these are encoded by genes within the major histocompatibility complex (MHC) on chromosome 6, and are called human leukocyte antigens (HLA). Genes that encode HLA antigens are highly polymorphic and tightly linked, with low recombination frequencies. They are inherited as a unit known as a haplotype one from each parent. Unrelated individuals are extremely unlikely to be matched, or to have sequence identity, at HLA loci. Within a family, however, each sibling has a 1 in 4 chance of inheriting the same HLA haplotypes as his/her sibling and therefore of having an HLA-matched donor. Conventional HLA typing of the recipient and donor involves characterization of the genes that encode the class I HLA-A and HLA-B antigens (by low- to intermediateresolution serological techniques), and of the HLA-DRB1 class II antigens (by highresolution molecular techniques). A potential donor with sequence identity to each of a patient s six HLA-A, HLA-B and DRB1 loci is referred to as 6/6 matched. If the patient is mismatched with the donor at one of these antigens, the patient is considered to be a 5/6 match with the donor. The importance of matching at additional HLA loci (HLA-C), along with high-resolution characterization of class I antigens, is being investigated in bone-marrow transplantation. As a source of haematopoietic progenitors for transplantation, cord blood has less alloreactivity than bone marrow, so grafts with limited HLA disparity (1 2 antigen mismatch) can be considered for transplantation. So, cord blood recipients will receive grafts that are 4/6 6/6 HLA matched (also designated 0 2/6 HLA mismatched). MAJOR HISTOCOMPATIBILITY ANTIGENS Antigens that are encoded by genes in the major histocompatibility complex on the short arm of chromosome 6. They are highly polymorphic and determine the immunological identity of the cell. In humans, they are also known as human leukocyte antigens (HLAs). therapeutic utility of these cells 10,12,13,20 prompted the creation of cord blood banks around the world. These act as repositories of HLA-typed units for the use of patients who require haematopoietic stem cells from unrelated donors There are now at least 100,000 cord blood units stored worldwide, and more than 2,000 cord blood transplants have been performed. Cord blood has unique properties compared with other sources of haematopoietic stem cells. Cord blood contains fewer nucleated cells/kg (by 1 2 logs) than bone marrow or mobilized peripheral blood. For example, the standard number of bone-marrow cells administered during a bone-marrow transplant is nucleated cells/kg ( CD34 + CELLS/kg and CD3 + T cells/kg). By contrast, only nucleated cord blood cells/kg ( CD34 + cells/kg and CD3 + T cells/kg) are typically transplanted into a paediatric patient. The fact that myeloid and lymphoid reconstitution occurs despite this low cell number indicates that cord blood is a potent source of haematopoietic stem cells. Interestingly, transplantation of cord blood has been associated with a lower than expected incidence of GVHD. The exact mechanism for this reduced alloreactivity is not fully understood. It could partly be due to the lower number of T cells that are present in cord blood. However, complex differences in the immune properties of cord blood are also likely to be involved. These include differences in cell phenotypes, the proliferative and cytotoxic responses of T cells, levels of cytokine production, and differences in natural-killercell and dendritic-cell biology 25. So, cord blood has unique potential as a source of haematopoietic progenitors for the treatment of cancer. Given that cord blood was previously considered a biological waste product, this represents a remarkable development in the history of haematopoietic stem-cell transplantation. Results of umbilical-cord transplantation Case-series related donor cord blood transplantation have been published by the International Bone Marrow Transplant Registry (IBMTR) 10 and the Eurocord Transplant Group 11. These have shown encouraging results, with survival rates of 61% for recipients of 0 1 HLA-antigen mismatched grafts at a median of 2 years after transplantation, and 63% at 1-year post-transplantation. This study prompted a comparison of cord blood and bone-marrow transplantation to HLA-identical related donors. Rocha et al. compared the outcomes of 113 recipients of HLA-identical cord blood transplants with those of 2,052 recipients of HLA-identical sibling bone marrow 26 (TABLE 1). They reported slower and lower incidence of haematopoietic recovery, but also lower rates of acute and chronic GVHD in children who received cord blood. However, the probability of survival 3 years after transplantation was comparable 64% in cord blood recipients versus 66% in bonemarrow recipients. The rates of cancer relapse were also similar for each group, despite the lower incidence of GVHD in recipients of cord blood. So, the findings of slower (and lower) incidence of haematopoietic recovery, but lower incidence of GVHD and of malignant relapse, as well as the comparable rates of survival, indicate that HLA-identical related donor cord blood is an acceptable alternative to bone marrow in the treatment of paediatric cancer patients. Given that most patients do not have a matched sibling donor, however, it is of greater practical CLASS 1 MATCHING Matching patients for HLA-A and HLA-B antigens. MYELOABLATIVE High-dose chemotherapy or chemotherapy with radiation that destroys (ablates) the haematopoietic system of the patient. CD34 + CELLS Immature haematopoietic progenitors. Table 1 Comparison of umbilical-cord blood transplantation with bone-marrow transplantation* Type of Days to Neutrophil Platelet % of patients % of patients % stem cell neutrophil recovery recovery develop who have surviving recovery % by day 60 % by day 180 grade II IV acute chronic patients GVHD by day 100 GVHD by after 3 years 3 years UCB cells 26 days 89% 86% 14% 6% 64% (n = 113) BM cells 18 days 98% 96% 24% 15% 66% (n = 2,052) BM cells, bone-marrow cells; GVHD, graft-versus-host disease; UCB cells, umbilical-cord blood cells. Adapted from REF. 26. *Cells derived from related donors; transplantation in paediatric patients. 528 JULY 2003 VOLUME 3

4 Table 2 Trials comparing umbilical-cord blood transplantation with bone-marrow transplantation* Number of patients % HLA-matched Survival Comments References patients in study 26 pairs for UCB versus BM; UCB: 16% UCB versus BM: Outcome of matched BM pairs for BM: 100% 53% versus 41% transplantation was UCB versus TCD UCB versus TCD: comparable to % versus 56% mismatched UCB transplantation 99 UCB UCB: 8% UCB: 35%* UCB patients had higher BM BM: 78% BM: 49%* risk characteristics; 180 TCD TCD: 57% TCD: 41%* overall mortality highest with TCD transplantation 296 UCB UCB: 6% 6/6 HLA UCB: 68% Outcome of 5/6 HLA-matched BM BM: 62% 5/6 HLA UCB: 46% UCB transplantation was less than 4/6 HLA comparable to that of UCB: 31% HLA-matched BM transplantation, 6/6 HLA BM: 46% but with a lower incidence of GVHD; 5/6 HLA BM: 40% outcome of 4/6 HLA-matched UCB transplantation was inferior to BM transplantation, but 6/6 HLA-matched UCB transplantation outcome was superior to that of BM transplantation BM, bone marrow; GVHD, graft-versus-host disease; HLA, human leukocyte antigen; TCD, bone marrow with T-cell depletion as method of GVHD prophylaxis; UCB, umbilical-cord blood. *Not adjusted for patient, disease and transplant differences. *Cells derived from unrelated donors; all trials in paediatric patients. TRANSPLANT-RELATED MORTALITY Death due to transplant complications such as GVHD or infection (in contrast to death from relapse of leukaemia). Also known as non-relapse mortality. importance to evaluate how umbilical-cord stem cells an bone-marrow cells compare when they are derived from an unrelated donor. Single institution and registry studies have shown that unrelated donor cord blood (1 2 HLA-antigen mismatched grafts) transplantation is associated with rapid availability, albeit slower haematopoietic recovery, as well as lower than expected incidence of severe acute and chronic GVHD. There has also been no indication of increased risk of malignant relapse in patients who received cord blood transplants, compared with patients who received bone-marrow transplants 10 18, Multiple studies have reported that cell dose is a crucial determinant of patient survival when cord blood comes from an unrelated donor 10,11,14,15,18,27,28. For example, the rate and likelihood of engraftment is decreased in recipients of cord blood grafts that contain fewer than 1.7 x 10 5 CD34 + cells/kg of the recipient s body weight 18. Donor engraftment was successful in only 72% of these patients, compared with 93% in those who received larger numbers of cells. TRANSPLANT-RELATED MORTALITY was 20% for patients who received greater than 1.7 x 10 5 CD34 + cells/kg, versus 75% for patients that received a cell dose below this threshold. Interestingly, Rubinstein et al. have reported that HLA mismatch also has a significant impact on cord blood transplant outcomes 15. In this study, donor neutrophils appeared in the blood of patients who received 6/6 HLA antigen (matched) cord blood grafts (n = 43) by 23 days after transplantation, compared with 28 days for patients who received mismatched grafts (n = 748). HLA disparity also affected the risk of severe acute GVHD, as 8% of 6/6 matched, 19% of 5/6 HLA matched and 28% of less than 4/6 HLA matched cord blood recipients developed severe GVHD. Overall, the probability of survival by 3 years after treatment was 27% for patients who were treated with umbilical-cord transplants for haematological malignancies. Adverse patient outcomes (defined as autologous reconstitution, requirement for a second transplant, and death) were independently associated with cord blood cell dose and HLA mismatch. Detailed results of different studies that compared the outcomes of unrelated donor cord blood and bone-marrow transplantation in children are shown in TABLE 2. In reviewing the results of unrelated donor haematopoietic transplantation studies, it is important to consider the complex variables that can affect the outcome of allogeneic transplantation (FIG. 1). For example, one advantage of cord blood is that it can be obtained substantially faster than unrelated bone marrow. However, it also means that many patients with high-risk cancers, who cannot wait the months required to identify an unrelated bone-marrow donor, are more likely to receive a cord blood transplant. This bias can render cord blood recipients at higher risk for adverse outcome, due to patient selection. Beyond the outcomes of haematopoietic recovery, GVHD and survival, there is much interest in the level of immune reconstitution after cord blood transplant. Thomson et al. reported that in 27 children who received cord blood transplants from unrelated donors, the natural-killer (NK)-cell population was reconstituted by 2 months post-transplantation, whereas the B-cell population took 6 months to recover, CD8 + T cells took 9 months and CD4 + T cells took 12 months 30. The authors concluded that this level of immune recovery was comparable to that seen after bone-marrow transplantation, and these results have been supported by subsequent studies 31,32.Klein et al. also studied T-cell immune reconstitution after cord blood transplantation, and found that normal numbers of thymic emigrants were detected by NATURE REVIEWS CANCER VOLUME 3 JULY

5 Table 3 Haematopoetic stem-cell sources* Bone marrow Umbilical-cord blood (using 6/6 HLA-matched donor) (using 4 6/6 HLA-matched donor) Advantages Large cell number available Rapid availability Faster engraftment Reduced incidence of GVHD Donor recall Less HLA restriction Ease of re-scheduling transplant day Lack of contamination with herpesvirus family Disadvantages Can cause severe GVHD Limited cell dose Lack of matched donors No donor recall Delay in availability Potential risk of genetic disease transmission GVHD, graft-versus-host disease; HLA, human leukocyte antigen. *Cells from unrelated donors. EVENT-FREE SURVIVAL The length of time after treatment that a person remains free of certain negative events, such as severe treatment side effects, cancer recurrence or progression, or death (from treatment side effects or from the cancer itself). 12 months post-transplantation in children, but that adult recipients experienced prolonged impairment of thymic recovery 33. How this compares with adult bone-marrow transplant recipients is unknown and requires further investigation. Notably, Weinberg et al. have shown that the factor that most adversely effects thymic recovery after haematopoietic stem-cell transplantation is GVHD 34. Therefore, cord blood transplant recipients could theoretically be at an advantage for immune reconstitution, compared with patients who received bone-marrow transplants, as cord blood is less likely to induce severe GVHD. There have been concerns that the low number of T cells and relative immunological naivete of cord blood could increase the risk for post-transplantation lymphoproliferative disorders especially in recipients of HLA-mismatched grafts. However, the incidence of lymphoproliferative disorders was only found to be 2% in a study of 272 recipients of cord blood from unrelated donors similar to that seen in recipients of unmanipulated bone-marrow cells from unrelated donors. This number is also lower than that reported for patients who received T-celldepleted bone-marrow grafts 35. Overall, further prospective studies are required to fully establish the relative merits of cord blood, compared with bone-marrow grafts. So far, published reports support the use of HLA-identical sibling or 0 2 HLA-antigen mismatched cord blood as an acceptable alternative to bone-marrow transplantation for the treatment of children with haematological malignancies. The relative merits of bone-marrow and cord blood transplantation as sources of haematopoietic stem cells are summarized in TABLE 3. Umbilical-cord blood transplantation in adults Multiple single institution and registry studies have shown that cell dose is a crucial determinant of haematopoietic recovery and survival after unrelated donor cord blood transplantation 10,11,14,15,18,27,28. Although large numbers of bone-marrow cells can safely be harvested from a single donor, the number of cord blood cells that can be collected is limited. The number of donor cells that are required for transplantation is calculated on the basis of the recipient s body weight adults (typical weight kgs) require larger numbers of cells than children (typical weight kg). So, the limited number of cells that can be obtained from cord blood is the main barrier to using them to treat adult patients. Laughlin et al. performed the first main study of cord blood transplantation in adults with haematological malignancies 36. They reported neutrophil recovery in 90% of patients by a median of 27 days after transplant. The incidence of severe acute GVHD was only 20% and the probability of EVENT-FREE SURVIVAL was 26% by 22 months after treatment. So, cord blood cells successfully engrafted in most adult patients without causing severe acute GVHD, and despite the low cell dose and level of HLA mismatch. Of the 68 patients studied, 17 eventually died from regimenrelated toxicity and 22 died of infection. This high incidence of transplant-related mortality was likely to be at least partly due to the high-risk patient population that was included in the study. Similar findings have been reported in adults with acute leukaemia who received unrelated donor bone-marrow transplants 37,38. Nonetheless, as with paediatric recipients, the umbilical-cord cell dose significantly influenced the likelihood of engraftment and survival. An important approach to improving the outcome of adult cord blood transplantation will therefore be to identify methods to increase the number of cord blood cells that are available for transplantation. Recent advances and future directions Although it is important to optimize cord blood collection techniques 39, the increase in cell number that can be achieved by such approaches is ultimately limited. Culture of cord blood cells in the laboratory before infusion into the patient, known as ex vivo expansion, is being investigated. However, this approach has met with limited success. There has been no clear evidence of haematopoietic stem-cell expansion in vitro, and patients who received ex vivo expanded cord blood samples have not shown an improved rate of neutrophil recovery Other approaches have involved co-transplantation of haplo-identical mesenchymal cells, which could potentially ameliorate damage to the bone-marrow microenvironment from high-dose chemoradiation and have been shown to be safe 44. However, so far, there has not been any demonstration of improved engraftment using this approach. The effects of the combined transplantation of two umbilical-cord blood units from different donors has been investigated as another strategy to augment cell dose 45. The logic is that due to cord blood s low level of alloreactivity, each donor-cell population will not reject the other, and the increased cell dose could enhance engraftment and patient survival. A pilot study has tested the safety of this approach in adults who are at high risk for relapse or transplant-related mortality. Patients received grafts that were mismatched in up to two HLA antigens to the recipient and to each other. 530 JULY 2003 VOLUME 3

6 Table 4 Recent advances and future directions Problem Solution Limited cell dose Increase cell dose by improving collection techniques; ex vivo expansion; co-infusion of multiple units Need for units with improved HLA match Increase size of banks and increase contributions from ethnic minority groups; some parents can create a matched donor for their child through in vitro fertilization and pre-implantation genetic analysis High incidence of transplant-related Increase cell dose; perform transplantation mortality in adults at earlier stage of cancer progression; dosereduced preparative regimens; more aggressive supportive care Lack of standardized banking practices Create central registry to facilitate and no central registry searches for matched donors; standardize banking practices, including viral testing, HLA typing and CD34 + cell enumeration PRE-IMPLANTATION GENETIC DIAGNOSIS The technique of testing for certain diseases or other attributes, such as HLA type, in an embryo. A high incidence of sustained donor-cell engraftment was reported, although the engrafted cells were derived from only one donor. Interestingly, given the relatively low cell number in the engrafted unit, the results seem to be better than what would have been predicted after transplantation of a single unit. Although these results will need to be confirmed, the safety of this approach has been shown, and, importantly, there was no increase in the incidence of acute GVHD, compared with single donor cord blood transplantation 45. Beyond cell dose, HLA disparity has also been shown to adversely impact patient survival after cord blood transplantation 15,18,27,28. To increase the number of HLA-matched potential donors, efforts are being made to increase cord blood collection among ethnic minorities particularly as minority patients are less likely to have unrelated bone-marrow donors available. For paediatric patients without an HLAmatched donor, parents might choose to conceive another child via in vitro fertilization, using PRE-IMPLANTATION GENETIC DIAGNOSIS to select an HLAmatched embryo. This approach has recently been pioneered at the University of Minnesota 46. Additional approaches will need to be developed to further improve survival of cord blood recipients. For example, by considering high-risk cancer patients for cord cell transplantation at an earlier stage before administration of other types of therapy and the development of refractory disease it might be possible to reduce the incidence of transplant-related mortality and cancer relapse. For older adults, those in poor health, or those with extensive previous therapy that are not able to tolerate high-dose chemoradiation, cord blood transplantation after lower dose ( reduced intensity or non-myeloablative ) chemoradiation is being investigated 47,48. Preliminary findings show that this approach has resulted in a high incidence of donor engraftment and a low incidence of severe acute GVHD 48. Although these early results are encouraging, further follow-up is required to assess the potency of the GVL effect. Finally, one of the highest priorities of cord blood researchers is to improve banking procedures. Despite the extensive use of cord blood in the clinic, practices such as unit identification, HLA typing, viral testing and CD34 + cell counting have not been standardized. The creation of a central registry that links all accredited cord blood banks would improve the ability of transplant centres to efficiently locate cord blood units. Current priorities in cord blood transplantation are summarized in TABLE 4. Current status Cord blood represents an exciting new haematopoietic stem-cell source for patients with haematological cancer, due to its rapid availability, reduced alloreactivity and low incidence of inducing severe GVHD. So far, there is no evidence that patients who have received cord blood transplants have an increased risk of cancer relapse compared with those who received bone-marrow transplants. The finding that children who have received bone-marrow transplants from unrelated donors have similar survival rates to those who receive cord blood transplants from unrelated donors has allowed umbilical-cord blood transplantation to become standard practice for the treatment of childhood leukaemia. If the reduced incidence of chronic GVHD but comparable risk of relapse is substantiated with a longer follow-up, cord blood transplantation could be found to provide patients with a significant advantage, in terms of quality of life, compared to bone-marrow transplantation. The treatment of adult leukaemia patients with unrelated donor haematopoietic stem cells is more complex. Patients with cancers other than chronic myelogenous leukaemia in the chronic phase have high rates of transplant-related mortality after receiving bone-marrow transplants from unrelated donors 37,38. The use of cord blood in these patients could have a significant advantage over bone marrow, in that it is less likely to induce severe GVHD although this advantage could be offset by the limited number of cells available. At this stage, the choice between bone marrow and cord blood transplantation must be individualized for each patient. Following referral for unrelated donor transplant, a search for both bone marrow and cord blood is appropriate. At the University of Minnesota, if the transplant is deemed urgent (that is, required within 3 months of referral), a strong preference is given to cord blood, provided that a unit with greater than cells/kg can be identified. The ultimate choice of stem-cell source ultimately depends on the availability of a suitable bone-marrow donor versus cord blood donor. Research and development of all aspects of cord blood transplantation from cord blood biology, to the clinical practice of cord blood transplantation, to banking procedures is proceeding rapidly. Although more prospective studies are needed in this field, this novel stem-cell source shows great promise in improving therapy for patients with haematological cancers. NATURE REVIEWS CANCER VOLUME 3 JULY

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Placental blood as a source of hematopoietic stem cells for transplantation into unrelated recipients. N. Engl. J. Med. 335, (1996). 13. Wagner, J. E. et al. Successful transplantation of HLAmatched and HLA-mismatched umbilical cord blood from unrelated donors: analysis of engraftment and acute graftversus-host disease. Blood 88, (1996). 14. Rubinstein, P. et al. Outcomes among 562 recipients of placental-blood transplants from unrelated donors. N. Engl. J. Med. 339, (1998). 15. Rubinstein, P. & Stevens, C. E. Placental blood for bone marrow replacement: the New York Blood Center s program and clinical results. Baillieres Best Pract. Res. Clin. Haematol. 13, (2000). 16. Barker, J. N. et al. Survival after transplantation of unrelated donor umbilical cord blood is comparable to that of human leukocyte antigen-matched unrelated donor bone marrow: results of a matched-pair analysis. Blood 97, (2001). 17. Rocha, V. et al. Comparison of outcomes of unrelated bone marrow and umbilical cord blood transplants in children with acute leukemia. Blood 97, (2001). 18. Wagner, J. E. et al. Transplantation of unrelated donor umbilical cord blood in 102 patients with malignant and nonmalignant diseases: influence of CD34 cell dose and HLA disparity on treatment-related mortality and survival. Blood 100, (2002). 19. Broxmeyer, H. in Cellular Characteristics of Cord Blood and Cord Blood Transplantation (ed. Broxmeyer, H.) 1 9 (AABB Press, Bethesda, Maryland, 1998). 20. Wagner, J. E., Kernan, N. A., Steinbuch, M., Broxmeyer, H. E. & Gluckman, E. Allogeneic sibling umbilical-cord-blood transplantation in children with malignant and non-malignant disease. Lancet 346, (1995). 21. Rubinstein, P., Rosenfield, R. E., Adamson, J. W. & Steven, C. E. Stored placental blood for unrelated bone marrow reconstitution. Blood 81, (1993). 22. Rubinstein, P. et al. Unrelated placental blood for bone marrow reconstitution: organization of the placental blood program. Blood Cells 20, (1994). 23. Peterson, R., Clay, M. & McCullough, J. in Cellular Characteristics of Cord Blood and Cord Blood Transplantation (ed. Broxmeyer, H.) (AABB Press, Bethesda, Maryland, 1998). 24. Gluckman, E. in Cellular Characteristics of Cord Blood and Cord Blood Transplantation (ed. Broxmeyer, H. E.) (ASBB Press, Bethesda, Maryland, 1998). 25. Roncarolo, M. et al. in Cellular Charaterisitcs of Cord Blood and Cord Blood Transplantation (ed. Broxmeyer, H.) (AABB Press, Bethesda, Maryland, 1998). 26. Rocha, V. et al. Graft-versus-host disease in children who have received a cord-blood or bone marrow transplant from an HLA-identical sibling. N. Engl. J. Med. 342, (2000). 27. Rubinstein, P. et al. Graft selection in unrelated placental/umbilical cord blood (PCB) transplantation: influence and weight of HLA match and cell dose on engraftment and survival. Blood 96, A588 (2000). 28. Rubinstein, P. et al. Comparison of unrelated cord blood and unrelated bone marrow transplants for leukemia in children: a collaborative study of the New York Blood Center and the International Bone Marrow Transplant Registry. Blood 98, A814 (2001). 29. Barker, J. N. et al. Searching for unrelated donor hematopoietic stem cells: availability and speed of umbilical cord blood versus bone marrow. Biol. Blood Marrow Transplant. 8, (2002). 30. Thomson, B. G. et al. Analysis of engraftment, graft-versushost disease, and immune recovery following unrelated donor cord blood transplantation. Blood 96, (2000). 31. Moretta, A. et al. Analysis of immune reconstitution in children undergoing cord blood transplantation. Exp. Hematol. 29, (2001). 32. Talvensaari, K. 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, (2002). 33. Klein, A. K. et al. T-Cell recovery in adults and children following umbilical cord blood transplantation. Biol. Blood Marrow Transplant. 7, (2001). 34. Weinberg, K. et al. Factors affecting thymic function after allogeneic hematopoietic stem cell transplantation. Blood 97, (2001). 35. Barker, J. N. et al. Low incidence of Epstein Barr virusassociated posttransplantation lymphoproliferative disorders in 272 unrelated-donor umbilical cord blood transplant recipients. Biol. Blood Marrow Transplant. 7, (2001). 36. Laughlin, M. J. et al. Hematopoietic engraftment and survival in adult recipients of umbilical-cord blood from unrelated donors. N. Engl. J. Med. 344, (2001). 37. Sierra, J. et al. Unrelated donor marrow transplantation for acute myeloid leukemia: an update of the Seattle experience. Bone Marrow Transplant. 26, (2000). 38. Barker, J. N. et al. Determinants of survival after human leucocyte antigen matched unrelated donor bone marrow transplantation in adults. Br. J. Haematol. 118, 1 7 (2002). 39. Ballen, K. K. et al. Bigger is better: maternal and neonatal predictors of hematopoietic potential of umbilical cord blood units. Bone Marrow Transplant. 27, 7 14 (2001). 40. McNiece, I., Kubegov, D., Kerzic, P., Shpall, E. J. & Gross, S. Increased expansion and differentiation of cord blood products using a two-step expansion culture. Exp. Hematol. 28, (2000). 41. Lewis, I. D. et al. Umbilical cord blood cells capable of engrafting in primary, secondary, and tertiary xenogeneic hosts are preserved after ex vivo culture in a noncontact system. Blood 97, (2001). 42. McNiece, I. K., Almeida Porada, G., Shpall, E. J. & Zanjani, E. Ex vivo expanded cord blood cells provide rapid engraftment in fetal sheep but lack long-term engrafting potential. Exp. Hematol. 30, (2002). 43. Shpall, E. J. et al. Transplantation of ex vivo expanded cord blood. Biol. Blood Marrow Transplant. 8, (2002). 44. MacMillan, M., Ramsey, N., Atkinson, K. & Wagner, J. Ex-vivo culture expanded parental haplo-identical mesenchymal stem cells (MSC) to promote engraftment in recipients of unrelated donor umbilical cord blood (UCB): results of a Phase I II clinical trial. Blood 100, A836 (2002). 45. Barker, J., Weisdorf, D., Defor, T., McGlave, P. & Wagner, J. Multiple unit umbilical cord blood transplantation in high risk adults with hematologic malignancies: analysis of engraftment and chimerism. Blood 100, A41 (2002). 46. Wagner, J. E., Auerbach, A. D. & Kahn, J. Embryo selection to create a genotypic identical hematopoietic stem cell (HSC) donor for a child with fanconi anemia (FA): transplant outcome and ethical implications. Blood 98, A744 (2001). 47. Rizzieri, D. A. et al. Successful allogeneic engraftment of mismatched unrelated cord blood following a nonmyeloablative preparative regimen. Blood 98, (2001). 48. Barker, J. N., Weisdorf, D. J., DeFor, T. E. & Wagner, J. E. Rapid and complete donor chimerism in adult recipients of unrelated donor umbilical cord blood transplantation after non-myeloablative conditioning. Blood 100, A42 (2002). Acknowledgements Supported by grants from the National Institutes of Health and the Children s Cancer Research Fund. Online links DATABASES The following terms in this article are linked online to: Cancer.gov: leukaemia renal-cell carcinoma LocusLink: CD4 CD8 CD34 DRB1 G-CSF HLA-A HLA-B HLA-C OMIM: Fanconi anaemia FURTHER INFORMATION Cord blood banks: Cord blood-bank operating procedures: http//:spitfire.emmes.com/study/cord/sop.htm Cord blood transplantation: Pre-implantation genetic diagnosis: Stem-cell research: www1.umn.edu/stemcell Access to this interactive links box is free online. 532 JULY 2003 VOLUME 3

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