Article Stem cell transplantation for thalassaemia
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1 RBMOnline - Vol 10. No Reproductive BioMedicine Online; on web 10 November 2004 Article Stem cell transplantation for thalassaemia Dr Javid Gaziev Javid Gaziev was an undergraduate and attended medical school at both the Medical University of Baku, in former USSR, and the University of Ancona, Italy. He was Hematology Fellow ( ) at the All Union Institute of Hematology and Blood Transfusion, Moscow. During he was Staff Physician in the Division of Hematology, Baku, transferring in 1990 to the Russian Central Hematology Centre, Moscow, to become Research Doctor of Medical Science in Hematology for one year. He has been the recipient of two fellowships: the Berloni Foundation Against Thalassemia Fellowship ( ) and the Research and Clinical Fellowship ( ), both at the Bone Marrow Transplantation Centre of Pesaro Hospital, Italy. The scientific degree of Doctor of Medical Sciences in Hematology was conferred on him in 1997 by the Russian Research Institute of Pediatric Hematology, Moscow. In 2002 Dr Gaziev became Senior Consultant Hematologist at the Bone Marrow Transplant Centre of Pesaro Hospital, Italy, and in 2003 these responsibilities were extended to the International Centre for Transplantation in Thalassemia and Sickle Cell Anemia, Mediterranean Institute of Hematology, Rome, Italy. Dr Gaziev has been author or co-author on 40 publications. Javid Gaziev 1, Guido Lucarelli Mediterranean Institute of Hematology, International Centre for Transplantation in Thalassemia and Sickle Cell Anemia, Azienda Ospedaliera San Camillo, Forlanini di Roma, Italy 1 Correspondence: San Camillo Hospital, Circonvallazione Gianicolense 87, Padiglione Marchiafava, Rome, Italy. Tel: ; Fax: ; j.gaziev@fondazioneime.org Abstract Although improvements in conventional treatment have enhanced the prognosis of thalassaemia, stem cell transplantation remains the only cure. Over the last 2 decades, progress in preventive strategies, effective control of transplant related complications and development of new preparative regimens, have considerably improved the results of transplants from HLA-identical siblings. Currently class 1, class 2 and class 3 patients receiving bone marrow transplantation (BMT) from an HLA-identical related donor have 87, 85 and 80% of probability of thalassaemia-free survival. The results of transplant in adult patients treated with current protocols are less successful. This study reports experience with BMT for thalassaemia. Keywords: late complications, stable mixed chimerism, stem cell transplantation, thalassaemia major Introduction Thalassaemia major is the most common transfusiondependent anaemia worldwide. The absent or extremely reduced production of the β-chain of haemoglobin causes severe ineffective erythropoiesis, massive erythroid hyperplasia in the bone marrow and extramedullary sites and haemolytic anaemia that requires lifelong transfusion therapy. Either ineffective erythropoiesis or chronic transfusion therapy leads to iron overload, resulting in endocrine deficiencies, cirrhosis, and cardiac disease in these Chronic transfusions and chelation with desferrioxamine have modified the natural course of thalassaemia major. Unfortunately, complications such as multiple endocrine dysfunctions, progressive liver disease, cardiac disease and post-transfusional viral infections are inevitable over time and lead to poor quality of life and increased mortality (Model et al., 2000; Li et al., 2002; Cunningham et al., 2004). Currently, the only proven therapeutic approach that can cure thalassaemia is allogeneic stem cell transplantation (SCT). Stem cell transplantation for β-thalassaemia major is an effective cure that is increasingly used worldwide, although in many countries where the disease is prevalent, only a tiny minority of patients have access to such a cure. Currently over 2000 patients have received SCT for β-thalassaemia major worldwide. As the goal of allogeneic SCT for thalassaemia is the substitution of the existing gene defect with the functioning gene of healthy or heterozygous donors through stem cells infused into the patient preceded by conditioning regimen, this procedure could be considered as allogeneic gene therapy. Stem cell transplantation for β-thalassaemia major Definition of risk classes Analysis of the results of bone marrow transplantation from HLA-identical family donors in the first 222 patients treated with busulfan (BU) 14 mg/kg and cyclophosphamide (CY) 111
2 mg/kg (BU14CY200) as conditioning regimen and cyclosporine (CSA) + methylprednisolone (MP) as graftversus-host disease (GVHD) prophylaxis revealed three adverse factors which had a negative influence on transplant outcome (Lucarelli et al., 1990; Giardini and Lucarelli, 1999). These risk factors are the presence of hepatomegaly of more than 2 cm, liver fibrosis or irregular iron chelation history (chelation was considered regular if it was started within 18 months after the first transfusion and was given as h/night subcutaneous infusion on at least 5 days per week, and any deviation from this regimen was considered as irregular). On the basis of these factors, patients are categorized into three risk classes: class 1 patients have none, class 2 patients have one or two and class 3 patients have all three risk factors. Class 1 patients These are younger patients without risk factors. Between October 1985 and January 2003, 146 class 1 patients with median age of 4 years (range 1 16 years) were given bone marrow transplantation following conditioning with Bu 3.5 mg/kg per day for 4 consecutive days and CY 50 mg/kg per day for the subsequent 4 days. GVHD prophylaxis consisted of CSA and MP for all but the last 37 patients, who received CSA, MP and a modified short course of MTX. The probabilities of overall survival, thalassaemia-free survival and rejection for these patients were 90, 87 and 3% respectively (Figure 1). Class 2 patients These patients have one or two risk factors as a consequence of poor transfusion therapy and/or irregular chelation. Three hundred and fifteen patients with median age of 9 years (range 2 16 years) were given a transplant after preparation with the same conditioning regimen used for class 1 They had overall survival, thalassaemia-free survival and rejection of 87, 85 and 3% respectively (Figure 2). Class 3 patients Class 3 younger patients (age <17 years), when treated with the same conditioning as class 1 and class 2 patients (BU14 mg/kg and CY200 mg/kg), showed a low probability of thalassaemia-free survival (53%) and a higher probability of non-rejection transplant related mortality (39%) (Lucarelli et al., 1996). The dose of cyclophosphamide was subsequently reduced to mg/kg in class 3 patients to overcome these complications (Lucarelli et al., 1996). In fact, these regimens in class 3 patients less than 17 years of age reduced the mortality rate, but the rejection rate increased from 13 to 35%, probably due to inadequate immunosuppression and failure to eradicate the massive erythroid hyperplasia characteristic of these Therefore, in April 1997, a new preparative regimen was started, intended to reduce erythroid expansion and increase immunosuppression over time to avoid unacceptable toxicity during the conditioning regimen (Sodani et al., 2004). According to this regimen, patients were given hydroxyurea (30 mg/kg per day) and azathioprine (3 mg/kg per day) from day 45 and fludarabine (20 mg/m 2 per day) from day 17 to 13 before transplant, along with hypertransfusions and intensive chelation with desferrioxamine. The conditioning regimen started on day 9 and consisted of BU14 mg/kg and CY 160 mg/kg for patients aged <17 years or 90 mg/kg for patients aged 17 years. As GVHD prophylaxis, they were given CSA, MP at 0.5 mg/kg per day, CY at 7.5 mg/kg on day 1 and MTX at 10 mg/m 2 on days 3 and 6 after transplantation. Analysis of the results of transplant in 38 class 3 patients aged <17 years and treated with this regimen showed a higher probability of survival and thalassaemia-free survival (94 and 80% respectively). Importantly, the rejection rate decreased from 30 to 14% (Figure 3). The preparative regimen was well tolerated without increasing toxicity. Adult patients Adult thalassaemia patients (age 17 years) have more advanced disease and treatment related organ complications, mainly due to prolonged exposure to iron overload. One hundred and seven patients with thalassaemia aged from 17 through 35 years were given transplant from HLA-identical siblings between November 1988 and September 1996 (Lucarelli et al., 1999). There were 13 class 2 and 74 class 3 All the class 2 patients received BU14CY200 as conditioning. Of the class 3 patients, 13 received BU16CY120, 18 received BU16CY160, and 43 received BU14CY160 as the conditioning regimen. As GVHD prophylaxis, the class 2 patients received CSA + MP while the class 3 patients were given CSA + MP in association with MTX. The probability of overall survival, thalassaemia-free survival, and rejection for entire group were 66, 62 and 4% respectively (Figure 4). The only factor significantly associated with outcome was the presence of chronic active hepatitis at the time of transplantation. Interestingly, unlike class 3 younger patients, reduced dose intensity of conditioning in adults was not associated with a higher rejection rate (4%), suggesting that donor host tolerance might be induced even among extensively transfused In fact, it has been shown that patients receiving more than 100 red cell transfusions before transplant experienced lower rejection than those who received fewer than 100 transfusions (24 versus 53% respectively). All but one adult patient received more than 100 transfusions. However, it is unlikely that this is the only influential factor, because the rejection incidence in younger patients receiving a lower CY dose was higher even in patients with a heavy transfusion history. Therefore, these results show that adult patients could be given less intensive transplant conditioning to overcome excessive transplant related toxicity. SCT from alternative donors Approximately 25 30% of patients can have an HLAidentical family donor. As SCT is the only available cure for thalassaemia, there is need to develop alternative stem cell sources such as matched from unrelated donors, partially matched or mismatched family donors or HLA identical siblings through preimplantation HLA typing. The results of historical experience of BMT from alternative donors for 29 patients with β-thalassaemia major who received phenotypically matched grafts or haploidentical grafts mismatched for one, two, or three antigens showed a higher graft failure rate (55%), and a low thalassaemia-free survival rate (21%) (Gaziev et al., 2000). Haploidentical-related
3 transplant using CD34 + positively selected cells is under study. Progress in molecular tissue-typing techniques and management of post-transplant complications enabled physicians to perform BMT for thalassaemia from unrelated donors. Thirty-two patients with thalassaemia received BMT from HLA-matched unrelated donors following BUCY ± thiotepa conditioning in different Italian transplant centres. Overall, the probability of thalassaemia-free survival was 66% and mortality was 25% (La Nasa et al., 2002). Thalassaemia-free survival was higher in class 1 and class 2 patients than in class 3 Patients sharing at least one extended haplotype had better survival. Graft-versus-host disease Acute and chronic GVHD was evaluated in 724 and 614 patients respectively receiving BMT from an HLA-identical related donor (Gaziev et al., 1997). The cumulative incidence of grade II IV acute GVHD in patients receiving CSA/MP or CSA/MP/MTX was 32 and 17% respectively. The overall incidence of chronic GVHD was 27.3%, with most patients developing a mild form of disease. The cumulative incidence of mild, moderate or severe chronic GVHD was 20, 8 and 2% respectively. Chimerism after transplant The data showed that 32.2% of patients at 2 months after myeloablative transplantation for thalassaemia had mixed chimerism (MC) (Lucarelli et al., 2002). The presence of MC in these patients is a risk factor for rejection, at least within 2 years after BMT. In fact, none of the patients with complete chimerism at 2 months had rejection, while 35 of 108 patients (32.4%) with MC determined at the same time lost their grafts. The number of residual host haematopoietic cells (RHC) determined at 2 months after BMT was predictive for graft rejection: patients with RHC of <10, and >25% had 13, 41 and nearly 100% rejection respectively (Andreani et al., 2000; Lucarelli et al., 2002). The incidence of persistent mixed chimerism was 10%. All these patients are transfusion-independent, indicating that in the case of established donor host tolerance few engrafted Figure 1. Kaplan Meier probability of survival, thalassaemiafree survival and cumulative incidence of rejection in class 1 Figure 2. Kaplan Meier probability of survival, thalassaemiafree survival and cumulative incidence of rejection in class 2 Figure 3. Kaplan Meier probability of survival, thalassaemiafree survival and cumulative incidence of rejection in class 3 Figure 4. Kaplan Meier probability of survival, thalassaemiafree survival and cumulative incidence of rejection in adult 113
4 114 donor cells can correct disease phenotype in patients with thalassaemia. Management of pre-existing iron overload and long-term complications of BMT Most thalassaemic patients after BMT continue to have endocrine dysfunction, cardiac disease, liver fibrosis due to iron overload and/or blood-borne viral infections acquired during conventional treatment. Therefore, the management of all of these complications after transplant is an important issue. It has been shown that iron stores after BMT remain elevated for years, especially in class 2 and class 3 patients (Lucarelli et al., 1993). Iron overload and hepatitis C virus infection are independent risk factors for liver fibrosis progression, and their concomitant presence results in a striking increase in risk (Angelucci et al., 2002). Therefore, the toxic effect of iron overload contributing to progression of varied organ damage already present should be avoided as soon as possible using post-transplant iron depletion. Both regular phlebotomy or chelation therapy can successfully remove excess iron from the body with normalization of the iron pool, which resulted in marked improvement in liver and cardiac function (Giardini et al., 1995; Angelucci et al., 1997; Mariotti et al., 1998; Muretto et al., 2002). Growth failure and endocrine dysfunction are common in medically treated thalassaemia major While the role of busulfan-containing regimens on growth velocity after transplant remains controversial the negative effect of this regimen on gonadal damage is well documented. Children receiving transplant before 8 years of age showed a normal growth rate, while older children, class III patients and patients who developed chronic GVHD had impaired growth (Gaziev et al., 1993). Gonadal damage is a common side effect of busulfan cyclophosphamide conditioning. Indeed, approximately one-third of boys and two-thirds of girls failed to spontaneously enter puberty following transplant (De Sanctis et al., 1997). Nevertheless, some patients can restore their fertility after transplant, which is supported by observations of two successful pregnancies and three spontaneous paternities (Gaziev and Lucarelli, 2003). BMT survivors are at risk for secondary malignancies, although the incidence of malignancies in patients was low (0.8%) (Gaziev et al., 2004). Three patients developed early and one late non-hodgkin lymphomas and four patients had solid tumours (spinocellular cancer, Kaposi s sarcoma, melanoma and colon cancer respectively). Four of these patients are alive and well. Conclusions Currently, BMT from an HLA-identical related donor offers to patients with thalassaemia a cure rate of 80 87% according to the class of risk. Patients with less advanced disease have better results that those with more advanced disease and age. Therefore, thalassaemia patients should be offered BMT at a younger age before they have developed disease and treatment related complications. As adult thalassaemia patients treated with myeloablative conditioning continue to have inferior results due to the advanced stage of their disease, they might be more suitable candidates for current fludarabine-based reduced intensity conditioning regimens. Careful selection of HLA-matched unrelated donors can increase the number of patients with thalassaemia benefiting from stem cell transplantation. One of the worrying complications of BMT is the development of chronic GVHD. Experience has shown that the incidence of clinically significant chronic GVHD is low in thalassaemia Further important issues are the fate of pre-existing conventional therapy related complications (such as iron overload, growth disturbances, endocrine complications, liver disease, cardiac disease) and the longterm complications of BMT. Pre-existing iron overload should be treated with either regular phlebotomy or chelation therapy with normalizing body iron stores which could arrest or reverse the progression of already existing organ damage. All BMT survivors should be regularly evaluated for long-term complications. References Andreani M, Nesci S, Lucarelli G et al Long-term survival of ex-thalassemic patients with persistent mixed chimerism after marrow transplantation. Bone Marrow Transplantation 25, Angelucci E, Muretto P, Lucarelli G et al Phlebotomy to reduce iron overload in patients cured of thalassemia by bone marrow transplantation. Italian Group for Phlebotomy Treatment of Transplanted Thalassemic Patients. Blood 90, Angelucci E, Muretto P, Nicolucci A et al Effects of iron overload and hepatitis C virus positivity in determining progression of liver fibrosis in thalassemia following bone marrow transplantation. Blood 100, Cunningham MJ, Macklin EA, Neufeld EJ, Cohen AR 2004 Complications of b-thalassemia major in North America. Blood 104, De Sanctis V, Galimberti M, Lucarelli G et al Growth and development in ex-thalassemic Bone Marrow Transplantation, 19 (Suppl. 2), Gaziev J, Lucarelli G 2003 Stem cell transplantation for hemoglobinopathies. Review. Current Opinion in Paediatrics 15, Gaziev D, Galimberti M, Giardini C et al Growth in children after bone marrow transplantation for thalassemia. Bone Marrow Transplantation 12 (Suppl. 1), Gaziev D, Polchi P, Galimberti M et al Graft-versus-host disease after bone marrow transplantation for thalassemia: an analysis of incidence and risk factors. Transplantation 63, Gaziev D, Galimberti M, Lucarelli G et al Bone marrow transplantation from alternative donors for thalassemia: HLAphenotypically identical relative and HLA-nonidentical sibling or parent transplant. Bone Marrow Transplantation 25, Gaziev J, Polchi P, Giardini C et al Malignant complications after BMT for thalassemia. Bone Marrow Transplantation 33, P791 Giardini C, Lucarelli G 1999 Bone marrow transplantation for betathalassemia. Hematology Oncology Clinics of North America 13, Giardini C, Galimberti M, Lucarelli G et al Desferrioxamine therapy accelerates clearance of iron deposits after bone marrow transplantation for thalassemia. British Journal of Haematology 89, La Nasa G, Giardini C, Argiolu F et al Unrelated donor marrow transplantation for thalassemia: the effect of extended haplotypes. Blood 99, Li CK, Luk CW, Ling SC et al Morbidity and mortality patterns of thalassemia major patients in Hong Kong: retrospective study. Hong Kong Medical Journal 8, Lucarelli G, Galimberti M, Polchi P et al Bone marrow
5 transplantation in patients with thalassemia. New England Journal of Medicine 322, Lucarelli G, Angelucci E, Giardini C et al Fate of iron stores in thalassemia after bone marrow transplantation. Lancet 342, Lucarelli G, Clift R, Galimberti M et al Marrow transplantation for patients with thalassemia: results in class 3 Blood 87, Lucarelli G, Galimberti M, Giardini C et al Bone marrow transplantation in adult thalassemic Blood 93, Lucarelli G, Andreani M, Angelucci E 2002 The cure of thalassemia by bone marrow transplantation. Blood Reviews 16, Mariotti E, Angelucci E, Agostini A et al Evaluation of cardiac status in iron-loaded thalassemia patients following bone marrow transplantation: improvement in cardiac function during reduction in iron burden. British Journal of Haematology 103, Modell B, Khan M, Darlison M 2000 Survival in beta-thalassemia major in the UK: data from the UK thalassemia registe. Lancet 10, Muretto P, Angelucci E, Lucarelli G 2002 Reversibility of cirrhosis in patients cured of thalassemia by bone marrow transplantation. Annals of Internal Medicine 136, Sodani P, Gaziev J, Polchi P et al New approach for bone marrow transplantation in patients with class 3 thalassemia aged younger than 17 years. Blood 104, Paper based on contribution presented at the International Meeting of Preimplantation HLA Typing and Stem Cell Transplantation in Cyprus, March, Received 31 August 2004; refereed 21 September 2004; accepted 27 October
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