Reduced-intensity conditioning hematopoietic SCT for pediatric patients with LAD-1: clinical efficacy and importance of chimerism
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1 (2012) 47, & 2012 Macmillan Publishers Limited All rights reserved /12 ORIGINAL ARTICLE Reduced-intensity conditioning hematopoietic SCT for pediatric patients with LAD-1: clinical efficacy and importance of chimerism AA Hamidieh 1, Z Pourpak 2, M Hosseinzadeh 1, MR Fazlollahi 2, K Alimoghaddam 1, M Movahedi 2, A Hosseini 1, Z Chavoshzadeh 3, M Jalili 1, S Arshi 4, M Moin 2 and A Ghavamzadeh 1 1 Hematology, Oncology and Stem Cell Transplantation Research Centre, Tehran University of Medical Sciences, Tehran, Iran; 2 Immunology, Asthma & Allergy Research Institute, Tehran University of Medical Sciences, Tehran, Iran; 3 Department of Pediatrics & Clinical Immunology, Mofid Children Hospital, Shahid Beheshti University of Medical Sciences, Tehran, Iran and 4 Department of Pediatrics & Clinical Immunology, Rasoul-e-Akram Hospital, Tehran University of Medical Sciences, Tehran, Iran Pediatric patients with leukocyte adhesion deficiency type-i (LAD-I) experience severe and recurrent lifethreatening bacterial infections with failure of pus formation and delayed wound healing. LAD-I is a rare inherited disease caused by mutation in the leukocyte CD18 integrin expression, resulting in defective adherence and migration of leukocytes, in particular neutrophilic granulocytes through the intravascular space. Hematopoietic SCT is the only curative treatment option available to patients with LAD-I. Since 2007, in a prospective trial, reduced-intensity conditioning regimen have been developed for 10 consecutive patients with LAD-I who were referred to our center. Based upon available data, it is the first time that such a number of patients affected by LAD-I have been treated with this regimen. This study attempts to show that reduced-intensity regimen leads to a favorable result in LAD-I patients even in those who have experienced comorbid complications. Following transplantation, some patients develop mixed chimerism, however, in our study mixed chimerism was not followed by transplant rejection. (2012) 47, ; doi: /bmt ; published online 11 July 2011 Keywords: leukocyte adhesion deficiency; hematopoietic SCT; reduced-intensity conditioning Introduction Leukocyte adhesion deficiency (LAD) is a rare inherited disorder, first described as a separate entity among the Correspondence: Professor AA Hamidieh, Department of Pediatric Hematology Oncology, Hematology-Oncology and Stem Cell Transplantation Research Center, Tehran University of Medical Sciences, Shariati Hospital, Kargar Avenue, Tehran 14114, Iran. aahamidieh@sina.tums.ac.ir Received 10 February 2011; revised 16 May 2011; accepted 30 May 2011; published online 11 July 2011 immunodeficiencies in A deficiency in leukocyte b2-integrin was recognized to be the cause of this syndrome in the early 1980s. Two distinct human disorders of LAD-I and LAD-II have been recognized. 2 4 LAD-I (the primary focus of our report) is the consequence of a heterogeneous mutation in the leukocyte b2-integrin (CD18) gene, which is located on chromosome 21. The b2-integrin a glycoprotein complex is required for adhesion dependant functions, such as aggregation, chemotaxis, phagocytosis, cell-mediated killing and adherence to vascular endothelium. 5 The severity of clinical presentation and complications in LAD-I correlate with the percentage of leukocytes demonstrating normal CD18 cell surface expression and/or degree of molecule deficiency. Children who suffer a moderate form of the disease have 1 10% normal cell surface expression of CD18, whereas severe LAD-I phenotypes express o1% normal cell surface expression of CD18. 6 Initial presentations include: omphalitis with delayed separation of umbilical cord and overwhelming septicemia. Later on patients develop nonpurulent, recurrent and necrotizing infections of the skin and mucous membranes, as well as persistent leukocytosis, gingivitis and periodontitis. 2 6 Hematopoietic SCT (HSCT) is the only known curative approach to LAD-I treatment Reduced intensity and myeloablative conditioning regimens are currently being used in the treatment of patients affected by LAD-I. Although full donor chimerism can be achieved with the use of myeloablative conditioning regimen, this regimen can lead to a higher risk of infections in patients with LAD-I who suffer from comorbid complications. 6 9 Recent data have shown that reduced-intensity conditioning (RIC) regimen, may lead to establishment of mixed chimerism in humans and canines following HSCT Despite this known fact, treatment based on RIC regimen because of its low transplant-related morbidity and mortality, has been increasingly utilized in recent years This study provides evaluation of RIC regimen, utilized in 10 LAD-1 patients who underwent HSCT at Hematology-Oncology and Stem Cell Transplantation research center (HORCSCT). Every single patient in our
2 study, who underwent the same RIC regimen, had variable amounts of chimerism. antithymocyte globulin (Atgam, Pfizer Inc, New York, NY, USA) 10 mg/kg for four consecutive days (days 4 to 1). 647 Patients and methods Patient characteristics This prospective study included 10 pediatric patients with LAD-I. Diagnosis in all patients was confirmed by flow cytometric analysis in peripheral blood cells. In all, 10 patients with LAD-I, who were candidates for HSCT, were referred to the HORCSCT in Shariati Hospital, between January 2007 and September The median age of patients at the time of transplantation was 2.7 years (range ). There were equal number of five girls and five boys. Eight patients had severe type of LAD-I and two had moderate form. The median period from the time of diagnosis of LAD-I to HSCT was 18 months (range 4 105). Various manifestations of the disease, such as: delayed separation of umbilical cord, persistent skin ulcers, gingival and periodontal infections and respiratory tract infections, were frequently observed during the pre-transplant period. Omphalitis and delayed umbilical separation were the most common and significant features. Leukocytosis persistently existed in all of patients from birth. Because of recurrent infections and extensive ulcers, the majority of our patients were admitted multiple times to receive medical treatment and also surgical debridement. However, these treatments seemed ineffective. Transplant preparation Adherence to the rules of ethics and protocols were uniformly observed. Signed informed consent by parents of patients was routinely required as a part of the inclusion criteria. A HLA-matched sibling is strongly advocated for donor selection in allogenic HSCT of LAD-I patients. To extend the use of allogeneic HSCT to patients without an HLA-matched sibling donor, we also investigated HSCT from other related donors. Low-resolution molecular typing for HLA-A and -B and -DRB1 were carried out for patients and their sibling. Moreover, high-resolution typing for class-i and II alleles was performed for recipient/ other related donor pairs. Unrelated cord blood stem cell or haplo-identical parent was considered as the last option for the treatment of LAD-I patients. Transplant procedure The graft was obtained from one of the three different sources: PBSCs, BM and umbilical cord blood. PBSC were obtained by continuous flow leukopheresis after mobilization by granulocyte CSF (G-CSF) and the BM was harvested under general anesthesia by aspiration into heparinized syringes from the marrow cavities of the iliac crests on the day of transplant. The protocol for conditioning transplant was approved by the HORCSCT Review Board and Ethics Committee in Shariati Hospital. Before stem cell infusion, all 10 patients received identical RIC regimen with combination of 30 mg/m 2 fludarabin administered i.v. for five consecutive days (days 8 to 4), melphalan 70 mg/m 2 i.v. for two consecutive days (days 3 and 2) and horse GVHD prophylaxis Prophylaxis against GVHD was performed via CsA 1.5 mg/kg. daily i.v. starting on day 1 then 3 mg/kg from day þ 7, plus methyl prednisolone 1 mg/kg i.v. starting on day 5 (day 5 to þ 7), then 0.5 mg/kg/day to day þ 14. CsA level was monitored twice weekly (therapeutic range ng/ml). Supportive care During hospitalization, all patients received the same supportive care. A total of 10 patients were cared for, in a similar isolation room with HEPA filter. Antimicrobial prophylaxis that was used during transplantation period, consisted of acyclovir mg/m 2 /day. It was i.v. started from day 10 to 1 then mg/m 2 /day. Acyclovir was given as prophylaxis for herpes simplex and VZV. In addition, trimethopim sulfamethoxazole was started from 10 to 1 then it continued from þ 36 to 2 years after transplant, it was used as Pneumocystis jiroveci prophylaxis. Itraconazole was administrated to prevent fungal infections for 3 months. All transfused blood products were irradiated before infusion. A total of patients received IVIg 0.5 g/kg every 3 weeks, but during infections it was given weekly. All patients received G-CSF at 5 mg/kg from day þ 8 until PMN counts recovered to /l. Blood samples from all patients were screened for CMV infection twice weekly. This test was based on quantitative CMV/DNA by PCR or CMV PP65 Ag. Any patient with positive result for CMV was treated with gancyclovir for 21 days, and the treatment was discontinued after the test became negative. Follow-up Disease statuses were monitored by flow cytometric detection of CD18-positive leukocytes in peripheral blood of the recipients monthly for 3 months, then followed up every 6 months. Chimerism evaluations (STR technique) were carried out on BM on days þ 15 and þ 30. Chimerism evaluations were also carried out on peripheral WBCs on days þ 60, þ 90, þ 180 and þ 365, respectively then followed up every 6 months. Definitions LAD-I consists of two subtypes: severe and moderate types. The severity of disease defined by the level of b2- subunit of CD18 expression on leukocytes; In the severe phenotype, which is usually associated with death during childhood, patients have o%1 normal cell surface expression of CD18; whereas in moderate phenotypes (o10% expression) patients have better prognosis and can survive to adulthood. 16,17 Mixed chimerism is defined by detection of 5 95% donor s HSC, in the recipient s BM or peripheral blood; full chimerism is quantified when 495% donor s HSC is detected in recipient s BM or peripheral blood Neutrophil engraftment is defined when ANC is 500/mL or greater on 3 consecutive days. Platelet engraftment is
3 648 defined when the platelet count exceeded /ml for 3 consecutive days unsupported by platelet transfusion. Acute GVHD (agvhd) and chronic GVHD (cgvhd) were scored according to standard criteria. 20,21 Results Patient and donor s characteristics The median age of patients and donors were 2. 7 years (range: ) and 21 years (range: 3 72), respectively. Median count of pre-transplant leukocytosis was (range: ) and median time of umbilical separation was 25 days (range: 15 45). Donor/recipient characteristics and transplant details are summarized in Table 1. Seven patients underwent SCT from HLAmatched-related donors, whereas the other patients underwent HSCT from HLA-mismatched-related or unrelated donors. The median number of infused PBSC-MNC and PBSC- CD34 was and /kg, respectively and the median number of infused BM-MNC and BM-CD34 was and /kg, respectively. Engraftment and chimerism All LAD-I patients but one were engrafted (90%). The median times to neutrophil and platelet engraftments were 11 days (range, 7 14), and 13 days (range, 10 32), respectively. Engraftment with full chimerism (495%) occurred in six patients. None of these patients had any symptoms of LAD-I disease during a follow-up period. The other three patients had mixed chimerism. At the latest follow-up time point the chimerism rate in two of them was 35%, and in the other one was 15%. These three patients with mixed chimerism feel well right now but a sustained mild leukocytosis exists in all of them. GVHD and infections Five out of 9 patients who achieved engraftment, developed agvhd. Three patients, who developed cgvhd, had a history of prior agvhd. The details of GVHD reported are specified in Table 2. We used same GVHD treatment, including: prednisolone 1 mg/kg/day and CsA as the first line treatment. Two patients who were refractory to first-line treatment were treated with Daclizumab 1 mg/kg. Patients, who developed agvhd, were successfully treated by the therapeutic approaches mentioned above, except one patient who died during treatment period. Four patients (44.4%) who developed CMV infection in the post-transplant period had a favorable response to ganciclovir therapy. The median time of treatment with ganciclovir was 25.5 days (range: 21 30). Outcome On the whole, the RIC regimen used in treatment of LAD-I patients was particularly well tolerated. The median time of Table 1 Patient and donor s characteristics Patient no. Sex Type of LAD Time from diagnosis to transplant (month) Age of transplant (month) Source of HSC Donor characteristics Age (years) Sex Relationship Matching 1 Female Severe 6 19 PB 29 Male Father Full 2 Female Severe PB 4.5 Female Sibling Full 3 Female Moderate PB 21 Male Sibling Full 4 Female Moderate PB 7 Male Sibling Full 5 Female Severe UCB Male Unrelated 5/6 6 Male Severe 8 13 PB 72 Male Grandfather Full 7 Male Severe PB 3 Male Sibling Full 8 Male Severe BM 27 Female Mother Haplo 9 Male Severe BM 30 Male Father 5/6 10 Male Severe 4 15 BM 20 Male Uncle Full Abbreviations: Haplo ¼ haploidentical; HSC ¼ hematopoietic SC; LAD ¼ leukocyte adhesion deficiency; PB ¼ peripheral blood; UCB ¼ umbilical cord blood. Table 2 Complication and outcome of LAD-I patient Patients no. Engraftment Chimerism Outcome/follow-up, month Day of engraftment of neutrophil Day of engraftment of plt agvhd (grade) cgvhd Infections after HSCT 1 Yes Mixed Alive/ Yes Mixed Alive/ Yes Full Alive/ Yes Full Alive/ III Limited CMV 5 No Death/4 6 Yes Full Alive/ III Limited CMV 7 Yes Full Alive/ IV CMV 8 Yes Full Death/ IV 9 Yes Full Alive/ IV CMV 10 Yes Mixed Alive/ Abbreviations: agvhd ¼ acute GVHD; cgvhd ¼ chronic GVHD; HSCT¼ hematopoietic SCT.
4 Overall survival Time (year) Figure 1 Cumulative OS of LAD-1 patients treated with the RIC regimen and allogeneic transplantation. and also different types of conditioning regimens used in different centers As pre-transplant infections in primary immunodeficiencies patients especially those affected by LAD-I lead to rise in mortality rate, 2 10 the use of less-toxic RIC as conditioning regimen seems to be highly effected in this regard. On the other hand, as LAD-I patients have hyperactive myeloid macrophage lineage, RIC regimen results in a high incidence of mixed chimerism and rejection in such affected patients In 2007, the first pediatric transplant unit was established in our center. As all of the patients referred to our center were found to be infected at the time of admission or transplantation, RIC regimen was used as the best treatment option for affected patients. According to the results of the study, RIC regimen is found to be safe and feasible therapeutic approach in the treatment of LAD-I patients. Recipients of RIC transplant, those with either full or mixed chimerism, had a long-term survival rate with no manifestation of LAD-I symptoms. It is also noticeable that the incidence of agvhd (grades III and IV), was significantly more common among patients in posttransplant period. This is probably because of the use of peripheral blood instead of BM as a stem cell source for transplantation. On the other hand, two patients who developed GVHD grade IV were not fully matched with their donors. 649 Figure 2 14-year-old girl diagnosed with moderate LAD and leg ulcer showing improvement after 4 months. Conflict of interest The authors declare no conflict of interest. follow-up was 27.4 months (range, ). The 3.7-year OS was 80% (Figure 1). Eight out of 10 (80%) patients who underwent HSCT are still alive and doing well at the time of this reporting. The HSCT recipients (n ¼ 8) who survive and remain engrafted continue to be free of any symptoms of infection. They also reflect the normal process of growth after transplantation. One patient (unrelated mismatched cord blood donor) died of sepsis 4 months after transplantation and the second patient (haplo-identical donor) died of agvhd and acute respiratory distress syndrome, 15 days after transplantation. Enlarging necrotic ulcers healed completely in three patients. Figure 2 shows leg ulcer in one of the patients in the pre-and post-transplant settings. Complication and outcome of LAD-I patient are summarized in Table 2. Discussion Recent studies have indicated that allogeneic HSCT is the only curative treatment for patients affected by LAD-I. 2 5 Although several articles have been published concerning the subject of transplantation in LAD-I patients, 4 6 there is no single unified agreement regarding choice of RIC or myeloablative conditioning regimen for treatment of patients. This can be concluded from a small number of patients who underwent transplantation around the world Acknowledgements We thank Dr Mohammad reza Ostadali, and we acknowledge the patients who participated in this study, the Hematology- Oncology and Stem Cell Transplantation Research Centre nursing staff and the referring doctors. References 1 Hayward AR, Harvey BA, Leonard J, Greenwood MC, Wood CB, Soothill JF. Delayed separation of the umbilical cord, widespread infections, and defective neutrophil mobility. Lancet 1979; 1: Qasim W, Cavazzana-Calvo M, Davies EG, Davis JM, Eames G et al. Allogeneic hematopoietic stem-cell transplantation for leukocyte adhesion deficiency. Pediatrics 2009; 123: Le Deist F, Blanche S, Keable H, Gaud C, Pham H, Descamp- Latscha B et al. Successful HLA nonidentical bone marrow transplantation in three patients with the leukocyte adhesion deficiency. Blood 1989; 74: Thomas C, Le Deist F, Cavazzana-Calvo M, Benkerrou M, Haddad E, Blanche S et al. Results of allogeneic bone marrow transplantation in patients with leukocyte adhesion deficiency. Blood 1995; 86: Bauer Jr TR, Creevy KE, Gu YC, Tuschong LM, Donahue RE, Metzger ME et al. Very low levels of donor CD18+ neutrophils following allogeneic hematopoietic stem cell
5 650 transplantation reverse the disease phenotype in canine leukocyte adhesion deficiency. Blood 2004; 103: Al-wahadneh AM, Haddadin I, Hamouri M, Omari K, Aejellat F. Bone marrow transplantation for leukocyte adhesion deficiency-i: case report. Saudi J Kidney Dis Transpl 2006; 17: Fischer A, Landais P, Friedrich W, Gerritsen B, Fasth A, Porta F et al. Bone marrow transplantation (BMT) in Europe for primary immunodeficiencies other than severe combined immunodeficiency: a report from the European Group for BMT and the European Group for Immunodeficiency. Blood 1994; 83: Burkholder TH, Colenda L, Tuschong LM, Starost MF, Bauer Jr TR, Hickstein DD. Reproductive capability in dogs with canine leukocyte adhesion deficiency treated with nonmyeloablative conditioning prior to allogeneic hematopoietic stem cell transplantation. Blood 2006; 108: Sokolic RA, Bauer TR, Gu YC, Hai M, Tuschong LM, Burkholder T et al. Nonmyeloablative conditioning with busulfan before matched littermate bone marrow transplantation results in reversal of the disease phenotype in canine leukocyte adhesion deficiency. Biol Blood Marrow Transplant 2005; 11: Hamidieh AA, Pourpak Z, Alimoghaddam K, Movahedi M, Bahoush G, Behmanesh F et al. Successful allogeneic stem cell transplantation with a reduced-intensity conditioning in a leukocyte adhesion deficiency type I patient. Pediatr Transplant 2009; 15: E30 E Bauer Jr TR, Gu YC, Tuschong LM, Burkholder T, Bacher JD, Starost MF et al. Nonmyeloablative hematopoietic stem cell transplantation corrects the disease phenotype in the canine model of leukocyte adhesion deficiency. Exp Hematol 2005; 33: Creevy KE, Bauer Jr TR, Tuschong LM, Embree LJ, Silverstone AM, Bacher JD et al. Mixed chimeric hematopoietic stem cell transplant reverses the disease phenotype in canine leukocyte adhesion deficiency. Vet Immunol Immunopathol 2003; 95: Mancias C, Infante AJ, Kamani NR. Matched unrelated donor bone marrow transplantation in leukocyte adhesion deficiency. Bone Marrow Transplant 1999; 24: Takahashi D, Nagatoshi Y, Saito Y, Inagaki J, Nagayama J, Shinkoda Y et al. Unrelated bone marrow transplantation using a reduced intensity-conditioning regimen in leukocyte adhesion deficiency. Bone Marrow Transplant 2006; 37: Gu YC, Bauer TR, Sokolic RA, Hai M, Tuschong LM, Burkholder T et al. Conversion of the severe to the moderate disease phenotype with donor leukocyte microchimerism in canine leukocyte adhesion deficiency. Bone Marrow Transplant 2006; 37: Engel ME, Hickstein DD, Bauer Jr TR, Calder C, Manes B, Frangoul H. Matched unrelated bone marrow transplantation with reduced-intensity conditioning for leukocyte adhesion deficiency. Bone Marrow Transplant 2006; 37: Farinha NJ, Duval M, Wagner E, Champagne J, Lapointe N, Barrette S et al. Unrelated bone marrow transplantation for leukocyte adhesion deficiency. Bone Marrow Transplant 2002; 30: Ozyurek E, Cowan MJ, Koerper MA, Baxter-Lowe LA, Dvorak CC, Horn BN. Increasing mixed chimerism and the risk of graft loss in children undergoing allogeneic hematopoietic stem cell transplantation for non-malignant disorders. Bone Marrow Transplant 2008; 42: Liesveld JL, Rothberg PG. Mixed chimerism in SCT: conflict or peaceful coexistence? Bone Marrow Transplant 2008; 42: Glucksberg H, Storb R, Fefer A, Buckner CD, Neiman PE, Clift RA et al. Clinical manifestations of graft-versus-host disease in human recipients of marrow from HL-A-matched sibling donors. Transplantation 1974; 18: Shulman HM, Sale GE, Lerner KG, Barker EA, Weiden PL, Sullivan K et al. Chronic cutaneous graft-versus-host disease in man. Am J Pathol 1978; 91:
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