M Ayas, H Solh, MM Mustafa, M Al-Mahr, I Al-Fawaz, A Al-Jefri, L Shalaby, A Al-Nasser and R Al-Sedairy
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1 (2001) 27, Nature Publishing Group All rights reserved /01 $ Bone marrow transplantation from matched siblings in patients with Fanconi anemia utilizing low-dose cyclophosphamide, thoracoabdominal radiation and antithymocyte globulin M Ayas, H Solh, MM Mustafa, M Al-Mahr, I Al-Fawaz, A Al-Jefri, L Shalaby, A Al-Nasser and R Al-Sedairy Department of Oncology, King Faisal Specialist Hospital and Research Center (KFSH&RC), Riyadh, Saudi Arabia Summary: Nineteen patients with Fanconi anemia (FA) and bone marrow failure underwent bone marrow transplantation (BMT) from matched siblings. Median age at BMT was 8.7 years. Conditioning consisted of low-dose cyclophosphamide (CY 5 mg/kg 4 days) and thoracoabdominal irradiation (TAI 400 cgy). Graft-versushost disease (GVHD) prophylaxis was cyclosporin A (CsA) in 13 patients and CsA plus methotrexate in 6 patients. Antithymocyte globulin (ATG) was added in the pretransplant as well as the post-transplant period. All patients received high-dose acyclovir from day 2 pre-bmt to day 28 post BMT, and intravenous immunoglobulins (IVIG), 500 mg/kg weekly from day 7 pre-bmt to day 90 post BMT. No fungal prophylaxis was given. All patients engrafted, (median, 14 days for an absolute neutrophil count /l; median, 37 days for platelet count /l). Fourteen (74%) patients are alive with sustained engraftment and are transfusion independent. Three (16.6%) patients developed acute GVHD; none developed chronic GVHD. Five (26%) patients developed invasive fungal infections, and two (10%) developed fatal CMV disease. We believe the addition of ATG may have contributed to the increased incidence of severe life-threatening fungal and viral infections in our series. Bone Marrow Transplantation (2001) 27, Keywords: bone marrow transplantation; Fanconi anemia; matched donors; antithymocyte globulins Fanconi s anemia (FA) is a rare genetic disorder characterized by progressive bone marrow failure, congenital abnormalities and a predisposition to malignancy. 1 6 Bone marrow transplantation is now considered the treatment of choice for severe marrow failure in patients with FA At the cellular level, FA cells are hypersensitive to DNA cross-linking agents, which results in chromosomal instability and cell death, 1,2 and at the clinical level this has Correspondence: Dr M Ayas, Department of Oncology, King Faisal Specialist Hospital and Research Center, MBC 64, PO Box 3354, Riyadh 11211, Saudi Arabia Received 17 July 2000; accepted 4 October 2000 translated into severe toxicity when conventional conditioning regimens were used in preparation of FA patients for BMT. 9,16 Several special conditioning regimens have been devised to account for the hypersensitivity of these patients to chemotherapeutic agents The group from Cincinnati reported their experience using low-dose cyclophosphamide (CY 5 mg/kg 4 days) and thoracoabdominal irradiation (TAI 400 cgy). In addition, antithymocyte globulin (ATG) was administered in the pretransplant period to promote engraftment, and in the post-transplant period for additional GVHD prophylaxis. 10 This regimen was well tolerated and was associated with a low incidence of complications including GVHD. We used the same protocol on 19 patients with FA and bone marrow failure. While our findings conform to those previously published, we observed a higher incidence of life-threatening infections. Patients and methods Patients Between April 1995 and March 1999, 19 patients (11 boys and eight girls) with confirmed FA received allogeneic bone marrow transplantation at KFSH&RC for bone marrow failure. The median age at diagnosis was 8 years (range, 1 10 years), and confirmation of the diagnosis of FA was made in all patients by documenting increased chromosomal breakage with diepoxybutane (DEB) and/or mitomycin-c. Before BMT, the median hemoglobin level was 7.9 g/dl (range, g/dl), the median absolute neutrophil count (ANC) was /l (range, /l) and the median platelet count was /l (range, /l). Four of the 19 patients had never received any packed red blood cell or platelet transfusions prior to BMT, four had received less than 10 transfusions, and the remaining 11 patients had received more than 10 transfusions in the year preceding the BMT. Median age at BMT was 8.7 years (range, 3 15 years), 12 patients had bone marrow examinations prior to BMT; none had evidence of dysplasia or leukemic transformation. Bone marrow cytogenetic analysis was done on four patients only; two had clonal chromosomal abnormalities (structural abnormality of the long arm of chromosome 1
2 140 in one patient and a marker chromosome in the other). All patients had normal chest X-rays before BMT and had no clinical evidence of infection. Donors All donors were HLA-identical siblings. The median age for donors was 13 years (range, 1 20 years), and all donors were tested for increased chromosomal breakage and found normal. CMV serology indicated that only two patients were CMV-seronegative, but their respective donors were CMVseropositive. Four of the donors were CMV-seronegative. Thus, all donor recipient pairs were CMV seropositive in at least one member. The harvested bone marrows (BM) were not manipulated, and the median CD34-positive cell count was (range, ) per kg recipient body weight. Preparative regimen The conditioning regimen consisted of cyclophosphamide (CY) 5 mg/kg once daily i.v. on days 5, 4, 3 and 2 pre-bmt (total dose 20 mg/kg), thoracoabdominal irradiation (TAI, 400 cgy) was given one day before BMT. The field of TAI extended from the angle of the mandible to the upper third of the thighs with shielding of kidneys posteriorly and of bladder anteriorly. Antithymocyte globulin (ATG) was given i.v. at a dose of 40 mg/kg on days 8, 6, 4, and 2 pre-bmt (total of four doses) and 20 mg/kg on days 2, 4, 6, 8, 10 and 12 post BMT (total of six doses). Graft-versus-host disease (GVHD) prophylaxis Thirteen patients received cyclosporin A alone and six received cyclosporin A and methotrexate at standard doses. 19 Supportive care All patients were treated in HEPA-filtered rooms and isolated until their ANC was greater than /l for 3 consecutive days. Intravenous immunoglobulin (IVIG) was administered weekly at a dose of 0.5 g/kg from day 7 until day +90. All patients received acyclovir 750 mg/m 2 /day from day 1 post BMT to day 28. All blood products were leukocyte-filtered and irradiated. No fungal prophylaxis and no pre-emptive or prophylactic ganciclovir were given. Results Engraftment Engraftment was defined as increase in the ANC to /l for 3 consecutive days. All 19 patients engrafted, and the median time was 14 days (range, days). The median time for a self-sustaining platelet count of /l was 37 days (range, days). Five patients (opposite sex BMT) had chimerism studies post BMT, and had evidence of a mixed chimerism profile. One of the two patients with abnormal clones pre-bmt had a cytogenetic analysis post BMT and had a normal donor karyotype. GVHD GVHD was graded according to published criteria. 20 Acute GVHD grade 2 was observed in three patients (16.6%) and all of them responded to treatment with steroids and cyclosporin A. None of the 16 at risk patients developed chronic GVHD. Toxicity All patients received broad spectrum antibiotic cover after transplant for febrile episodes, and bacteremia was documented in 11 patients. However, the major toxicity post BMT was the development of life-threatening CMV and fungal infections. A total of five patients had evidence of fungal infection. Two patients had pulmonary aspergillosis proven by biopsy and both died before day 100. In one of them, however, the immediate cause of death was intracranial hemorrhage. One patient had biopsy-proven hepatosplenic candidiasis and recovered after antifungal therapy. The remaining two patients had presumed pulmonary fungal infections. No biopsy was done due to parental refusal, but there was strong radiological suspicion on chest CT. They received antifungal therapy and the lesions resolved. Two patients developed disseminated CMV infection before day 100 that led to bone marrow failure after initial engraftment; the diagnosis was established by a positive CMV antigenemia test and deteriorating clinical status. Both patients subsequently died from multi-system failure. In one of these two patients, the CMV infection was concomitant with pulmonary aspergillosis. A third patient had a positive CMV antigenemia test with elevated liver enzymes, but was clinically stable. She was treated with ganciclovir and responded well. Two patients developed mild, self-limited veno-occlusive disease of the liver. One patient developed hemorrhagic cystitis that resolved within a few days; the patient was managed with hydration only. Mucositis, grade 2, developed in 11 patients (oral mucositis was scored from grade 1 to 3, depending on redness, ulceration and ability to eat). 21 All patients were managed with i.v. analgesia and parenteral alimentation. A total of 11 patients (58%) developed hypertension (blood pressure greater than 95th percentile for age) during BMT, requiring short-term antihypertensive treatment. Malignancy One patient developed squamous cell carcinoma of the tongue 57 months post BMT. He underwent partial glossectomy with cervical lymph node dissection and is currently alive but the follow-up time is still short (6 weeks).
3 Follow-up Fourteen of the 19 patients (74%) are alive with sustained engraftment, at a median follow up time of 20 months (range months), for an actuarial overall survival of 66% at 4 years (Figure 1). One patient died from an intracranial hemorrhage on day 50 post BMT despite evidence of engraftment. Two patients lost their grafts fairly early in their course (before day 100); the graft failure was associated with disseminated CMV infection in both cases, and both patients subsequently died from multisystem failure. The fourth death was a female patient who became transfusion dependent once again about 6 months post BMT. Chimerism analysis then was still consistent with donor cells (opposite sex BMT), and she developed acute myeloid leukemia about 18 months after BMT and eventually succumbed to it. The fifth patient initially had good engraftment but developed neutropenia about 3 months after BMT. His bone marrow showed good left shifted granulopoesis suggestive of peripheral destruction, and chimerism analysis confirmed donor cells (opposite sex BMT). However, the patient was poorly compliant with his clinic visits was admitted to his local hospital for fever and neutropenia and died of overwhelming Klebsiella pneumoniae sepsis 1 year after BMT. Discussion The development of well tolerated, immunosuppressive preparative regimens for patients undergoing BMT has proven to be a rather challenging task for hematologists. This is even more relevant in patients with FA whose underlying increased chromosomal fragility makes them extremely susceptible to chemotherapy and radiation toxicity Patients with FA usually suffer from progressive bone marrow failure, with aplasia developing at a mean age of 6.2 years and acute leukemia developing at a mean age of 14.4 years, 1 which makes BMT an attractive curative measure for the bone marrow failure. Early reports of BMT in FA patients used conditioning regimens similar to those used in aplastic anemia, which led to severe toxicity. 9 The Seattle group used a nonradiationcontaining regimen consisting of high-dose cyclophos- Cum survival Time (in months) Figure 1 Actuarial survival in 19 patients who underwent BMT using low-dose CY, TAI and ATG phamide ( mg/kg) in 12 patients, and although all patients engrafted, the regimen was associated with severe toxicity (severe mucositis and hemorrhagic cystitis). 16,17 Furthermore, significant acute GVHD developed in four patients (33%), and extensive chronic GVHD occurred in four (50%) of eight patients at risk. A total of seven (65%) patients were alive at a median of 5 years after BMT. Based on in vitro evidence of increased frequency of chromosomal breakage in lymphocytes from patients with FA when they were incubated with serum from a cyclophosphamide-treated patient, 22 and based on data showing increased skin radiosensitivity of FA patients before BMT, 23,24 the French group used a lower dose of cyclophosphamide (20 mg/kg) over 4 days and TAI 500 cgy in 50 patients, which resulted in successful engraftment. 13 The survival estimate was 74.4% at 54 months and 58.5% at 100 months. This regimen was, however, associated with a significantly high rate of acute GVHD (55%), as well as chronic GVHD (69.9%). Kohli-Kumar and colleagues 10 modified the Gluckman regimen by adding antithymocyte globulins in the pre-transplant period in an effort to enhance engraftment and in the post-transplant period to reduce the risk for GVHD. Eighteen patients were transplanted, and all engrafted. Engraftment was rapid with a median time of 12 days to an ANC /l, and a median time of 22 days to achieve a self-sustained platelet count of /l. The regimen was well tolerated; mucositis was the only significant complication. No acute GVHD was observed, but three patients developed limited chronic GVHD. One patient had delayed graft failure but was rescued with a repeat BM infusion after reconditioning with ATG. Based on the good results reported by Kohli-Kumar s group, we adopted their regimen and report here our results in 19 FA patients with bone marrow failure transplanted with this regimen. Our results confirmed their findings; good engraftment with low incidence of both acute and chronic GVHD. The main complication of concern in our patients was the development of fatal fungal and viral infections. In their series, Kohli-Kumar et al reported no cases of CMV disease, but half of the 18 patient/recipient pairs were CMV seronegative. The use of ATG in the preparative regimen before and after the BM infusion has helped to more selectively target the cells essential for graft rejection and GVHD, and this was translated clinically into a lower incidence of both, yet the increased risk for opportunistic infections in the posttransplant period emerged as a major complication. Experience in solid organ transplantation has shown that conventional immunosuppression is associated with a low risk of CMV disease (10%), and that the risk rose to 64% when anti-lymphocyte antibody therapy was administered to treat rejection. Furthermore, the data showed that, in renal transplant recipients who were CMV seropositive, the use of pre-emptive ganciclovir therapy during treatment with antilymphocyte antibodies significantly reduced the incidence of CMV disease. 25,26 Although the exact mechanisms of host defense against fungal infections are not well understood, there are emerging data to indicate that T cell function may be important. Furthermore, it has been shown in a mouse model that 141
4 142 CD8-positive cells are necessary for optimal clearance of the fungus from tissues of mice infected with Paracoccidioidomycosis. 27 ATG is known to be a lymphocyte-selective immunosuppressant, and recent studies have shown that it specifically inhibits CD8-positive cells. 28 Other opportunistic infections, such as CMV may also have predisposed our patients to the development of pulmonary aspergillosis. Because of our results, we have started using prophylactic fluconazole on all FA patients undergoing BMT but further studies utilizing lower doses of ATG should be considered. Thus far, only one of our patients developed a secondary malignancy, but our follow-up time is too short to reach any solid conclusions regarding the risks of development of secondary malignancy in these patients. It has been suggested that the use of irradiation as part of the conditioning regimen is a significant risk factor for secondary malignancy among patients undergoing BMT for non-fanconi aplastic anemia This risk could theoretically be higher in patients with FA because of their chromosomal instability and defective DNA repair mechanisms. We believe that the role of radiation therapy in the conditioning regimens for FA patients is still not well delineated, and the use of non radiation-containing regimens should be considered to lessen the potential risk of secondary malignancy. Medeiros et al 11 showed that decreasing the dose of cyclophosphamide to 100 mg/kg over 4 days resulted in successful engraftment and was associated with acceptable toxicity. Using this regimen, Medeiros reported a survival of 88% in 16 patients with FA transplanted from matched sibling donors. Acute and chronic GVHD were observed in 13% and 7% of patients, respectively. We have recently started a new protocol for conditioning of FA patients undergoing BMT using a higher dose of CY (15 mg/kg/day 4 days) and ATG but without radiation therapy. Acknowledgements We are extremely grateful to Dr Robert Stuart, (chairman of the Department of Oncology at the King Faisal Specialist Hospital) for his critical review of this manuscript. We are also grateful to Mrs Saada Mansour (clinical research coordinator) and to Mrs Cynthia Magpantay (research data analyst) for their excellent assistance in the data collection and analysis. References 1 Auerbach AD, Allen RG. Leukemia and preleukemia in Fanconi anemia patients. A review of the literature and report of the international Fanconi anemia registry. Cancer Genet Cytogenet 1991; 51: Alter BP, Young NS. The bone marrow failure syndromes. In: Nathan DG, Oski FA (eds). Hematology of Infancy and Childhood, Vol 1. Saunders: Philadelphia, PA, 1998, pp Alter B. Fanconi s anemia, current concepts. Am J Pediatr Hematol Oncol 1992; 14: Alter B. Fanconi s anemia and its variability. Br J Haematol 1993; 85: Liu JM, Buchwald M, Walsh CE, Young NS. Fanconi anemia and novel strategies for therapy. Blood 1994; 84: Butturini A, Gale RP, Verlander PC et al. Hematologic abnormalities in Fanconi anemia: an International Fanconi Anemia Registry study. Blood 1994; 84: Gluckman E, Berger R, Dutreix J. Bone marrow transplantation for Fanconi anemia. Semin Hematol 1984; 21: Gluckman E. Allogeneic bone marrow transplantation in Fanconi anemia. Bone Marrow Transplant 1996; 18 (Suppl. 3): Gluckman E, Devergie A, Schaison G et al. Bone marrow transplantation in Fanconi anaemia. Br J Haematol 1980; 45: Kohli-Kumar M, Morris C, DeLaat C et al. Bone marrow transplantation in Fanconi anemia using matched sibling donors. Blood 1994; 84: Medeiros CR, Zanis-Neto J, Pasquini R. Bone marrow transplantation for patients with Fanconi anemia: reduced doses of cyclophosphamide without irradiation as conditioning. Bone Marrow Transplant 1999; 24: Zwaan C, Van Weel-Sipman M, Fibbe W et al. Unrelated donor bone marrow transplantation in Fanconi anaemia: the Leiden experience. Bone Marrow Transplant 1998; 21: Socié G, Devergie A, Girinski T et al. Transplantation for Fanconi s anaemia: long term follow-up of fifty patients transplanted from a sibling donor after low-dose cyclophosphamide and thoraco-abdominal irradiation for conditioning. Br J Haematol 1998; 103: Zanis-Neto J, Ribeiro RC, Medeiros C et al. Bone marrow transplantation for patients with Fanconi anemia: a study of 24 cases from a single institution. Bone Marrow Transplant 1995; 15: Yabe M, Yabe H, Matsuda M et al. Bone marrow transplantation for Fanconi anemia, adjustment of the dose of cyclophosphamide for preconditioning. Am J Pediatr Hematol Oncol 1993; 15: Flowers M, Doney KC, Storb R et al. Marrow transplantation for Fanconi anemia with or without leukemic transformation: an update of the Seattle experience. Bone Marrow Transplant 1992; 9: Flowers M, Zanis J, Pasquini R et al. Marrow transplantation for Fanconi anaemia: conditioning with reduced doses of cyclophosphamide without radiation. Br J Haematol 1996; 92: Gluckman E, Auerbach A.D, Horowitz M et al. Bone marrow transplantation for Fanconi anemia. Blood 1995; 86: Storb R, Deeg HJ, Pepe M et al. Graft-versus-host disease prevention by methotrexate combined with cyclosporin compared to methotrexate alone in patients given marrow grafts for severe aplastic anaemia: long-term follow-up of a controlled trial. Br J Haematol 1989; 72: Thomas ED, Storb R, Clift RA et al. Bone marrow transplantation (second of two parts). New Engl J Med 1975; 292: Ferretti GA, Ash RC, Brown AT et al. Chlorhexidine for prophylaxis against oral infectious and associated complications in patients receiving bone marrow transplantation. J Am Dent Assoc 1987; 114: Berger R, Bernheim A, Gluckman E, Gisselbrecht C. In vitro effect of cyclophosphamide metabolites on chromosomes of Fanconi anaemia patients. Br J Haematol 1980; 45: Gluckman E, Devergie A, Dutreix J. Radiosensitivity in Fanconi anaemia: application to the conditioning regimen for bone marrow transplantation. Br J Haematol 1983; 54: Gluckman E. Radiosensitivity in Fanconi anemia: application
5 to the conditioning for bone marrow transplantation. Radiother Oncol 1990; 18 (Suppl. 1): Hibberd P, Tolkoff-Rubin N, Conti D et al. Preemptive ganciclovir therapy to prevent cytomegalovirus disease in antibody-positive renal transplant recipients. Ann Intern Med 1995; 123: Pascual M, Rubin R, Cosimi A. Minimizing the toxicity of antilymphocyte antibody therapy. Transplant Proc 1996; 28: Cano LE, Singer-Vermes LM, Costa TA et al. Depletion of CD8 (+) T cells in vivo impairs host defense of mice resistant and susceptible to pulmonary paracoccidioidomycosis. Infect Immun 2000; 68: Teramura M, Kobayashi S, Iwabe K et al. Mechanism of action of antithymocyte globulin in the treatment of aplastic anaemia: in vitro evidence for the presence of immunosuppressive mechanism. Br J Haematol 1997; 96: Socié G, Henry-Amar M, Cosset JM et al. Increased incidence of solid malignant tumors after bone marrow transplantation for severe aplastic anemia. Blood 1991; 74: Pierga JY, Socie G, Gluckman E et al. Secondary solid malignant tumors occurring after bone marrow transplantation for severe aplastic anemia given thoraco-abdominal irradiation. Radiother Oncol 1994; 30: Deeg HJ, Socié G, Schoch G et al. Malignancies after marrow transplantation for aplastic anemia and Fanconi anemia: a joint Seattle and Paris analysis of results in 700 patients. Blood 1996; 87:
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