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1 Supplementary Appendix This appendix has been provided by the authors to give readers additional information about their work. Supplement to: Pai S-Y, Logan BR, Griffith LM, et al. Transplantation outcomes for severe combined immunodeficiency, N Engl J Med 2014;371: DOI: /NEJMoa
2 Transplantation of 240 patients with Severe Combined Immunodeficiency (SCID) from : A Primary Immune Deficiency Treatment Consortium report Supplementary Appendix Sung-Yun Pai, 1 Brent R. Logan, 2 Linda M. Griffith, 4 Rebecca H. Buckley, 5 Roberta E. Parrott, 5 Christopher C. Dvorak, 6 Neena Kapoor, 7 Imelda C. Hanson, 8 Alexandra H. Filipovich, 9 Soma Jyonouchi, 10 Kathleen E. Sullivan, 10 Trudy N. Small, 3 Lauri Burroughs, 11 Suzanne Skoda-Smith, 11 Ann E. Haight, 12,13 Audrey Grizzle, 12 Michael A. Pulsipher, 14 Ka Wah Chan, 15 Ramsay L. Fuleihan, 16 Elie Haddad, 17 Brett Loechelt, 18 Victor M. Aquino, 19 Alfred Gillio, 20 Jeffrey Davis, 21 Alan Knutsen, 22 Angela R. Smith, 23 Theodore B. Moore, 24 Marlis L. Schroeder, 25 Frederick D. Goldman, 26 James A. Connelly, 27 Matthew H. Porteus, 28 Qun Xiang, 2 William T. Shearer, 8 Thomas A. Fleisher, 29 Donald B. Kohn, 24 Jennifer M. Puck, 6 Luigi D. Notarangelo, 30 Morton J. Cowan, 6 Richard J. O Reilly 3 (corresponding) 1 Boston Children s Hospital, Division of Pediatric Hematology-Oncology and Dana- Farber Cancer Institute, Department of Pediatric Oncology, Boston, MA, USA 2 Medical College of Wisconsin, Division of Biostatistics, Milwaukee, WI, USA 3 Memorial Sloan-Kettering Cancer Center, Bone Marrow Transplant Program, New York, NY, USA 4 National Institutes of Health, National Institute of Allergy and Infectious Diseases, Division of Allergy, Immunology and Transplantation, Bethesda, MD, USA 5 Duke University Medical Center, Departments of Pediatrics and Immunology, Durham, NC, USA 6 Benioff Children s Hospital, Division of Allergy/Immunology/Blood & Marrow Transplantation, University of California San Francisco, San Francisco, CA, USA 7 Children s Hospital Los Angeles, Department of Pediatrics, Los Angeles, CA, USA 8 Baylor College of Medicine, Texas Children s Hospital, Section of Pediatric Immunology, Allergy and Rheumatology, Houston, TX, USA 9 Cincinnati Children s Hospital Medical Center, Bone Marrow Transplantation and Immunodeficiency, Cincinnati, OH, USA 10 Children s Hospital of Philadelphia, Department of Pediatrics, Philadelphia, PA, USA 11 Fred Hutchinson Cancer Research Center, Seattle Children s Hospital, Clinical Research Division, Seattle, WA, USA 12 Children s Healthcare of Atlanta, Aflac Cancer and Blood Disorders Center, Atlanta, GA, USA 13 Emory University School of Medicine, Atlanta, GA, USA 14 Primary Children s Hospital, Division of Hematology, University of Utah/Huntsman Cancer Institute, Salt Lake City, UT, USA 15 Texas Transplant Institute and Methodist Children s Hospital of South Texas, San Antonio, Texas, USA 1
3 16 Ann & Robert H. Lurie Children s Hospital of Chicago, Northwestern University Feinberg School of Medicine, Chicago, IL, USA 17 University of Montreal, CHU Sainte-Justine, Montreal, QC, Canada 18 Children s National Medical Center, Division of Blood and Marrow Transplantation & Allergy and Immunology, Washington, DC, USA 19 University of Texas Southwestern Medical Center, Department of Pediatrics, Dallas, TX, USA 20 Hackensack University Medical Center, Pediatric Blood and Marrow Transplant Program, Hackensack, NJ, USA 21 BC Children s Hospital and BC Women s Hospital and Health Center, Department of Pediatrics, Vancouver, BC, Canada 22 Cardinal Glennon Children s Medical Center, Division of Pediatric Allergy & Immunology, Saint Louis University, Saint Louis, MO, USA 23 University of Minnesota, Division of Pediatric Blood and Marrow Transplantation, Minneapolis, MN, USA 24 University of California, Los Angeles, Mattel Children s Hospital, Los Angeles, CA, USA 25 University of Manitoba, Department of Pediatrics and Child Health, Winnipeg, MB, Canada 26 Children s of Alabama, University of Alabama Birmingham, Department of Pediatrics, Birmingham, AL, USA 27 University of Michigan, Department of Pediatric Hematology-Oncology, Ann Arbor, MI, USA 28 Stanford University, Division of Hematology/Oncology/Stem Cell Transplantation, Stanford, CA, USA 29 National Institutes of Health, Clinical Center, Department of Laboratory Medicine, Bethesda, MD, USA 30 Boston Children s Hospital, Division of Immunology, Manton Center for Orphan Disease Research, Harvard Stem Cell Institute, Boston, MA, USA Corresponding author: Richard J. O Reilly Memorial Sloan-Kettering Cancer Center 1275 York Avenue New York, NY Tel: oreillyr@mskcc.org 2
4 Table of Contents Supplemental Methods 4 Figure S1 5 Figure S2 6 Figure S3 7 Tables 8-16 Table S1: Conditioning regimens 8 Table S2: Patient characteristics 9 Table S3: Factors associated with age at transplant 10 Table S4: Probabilities of graft failure by donor type and genotype 10 Table S5: Incidence of GVHD by donor type 11 Table S6: Causes of death after transplant 13 Table S7: Multivariate analysis of immune reconstitution 14 Table S8: Association of full or mixed donor chimerism with various factors 16 References 17 3
5 Supplemental Methods Each center submitted coded data on all SCID patients who undergone allogeneic HSCT, adenosine deaminase enzyme replacement therapy or gene therapy at their center between January 1, 2000 and December 31, Patients were considered according to consensus criteria that the PIDTC has established for different types of SCID. 1 These included 1. classic SCID (absolute T-cell count <300 and absence of significant T-cell responses to the mitogen phytohemagglutinin, or the presence of maternally engrafted T- cells), 2. leaky SCID (those with low but detectable responses to mitogens and oligoclonal T-cell populations), 3. Omenn s syndrome, and 4. reticular dysgenesis. An expert panel (R.H.B., M.J.C., T.A.F., L.M.G., D.B.K., L.D.N., R.J.O, S.-Y.P., J.M.P., W.T.S.) reviewed each submitted case and deemed 285 patients to meet criteria for SCID. This paper analyzes the subset of patients who had classic SCID and underwent allogeneic transplant, numbering 240. The other 45 patients included 21 with leaky SCID, 13 with Omenn s syndrome, 2 with reticular dysgenesis and 9 who either received enzyme replacement therapy as the first treatment or who underwent gene therapy. The study was designed by R.J.O., R.H.B., M.J.C., T.A.F., B.R.L., L.M.G., L.D.N., D.B.K., S.-Y.P., J.M.P., W.T.S. The data were gathered by V.M.A., R.H.B., L.B., J.A.C., K.W.C., M.J.C., J.D., C.C.D., A.H.F., R.L.F., A.G., F.D.G., E.H., A.H., I.C.H., S.J., N.K., A.K., D.B.K., B.L., T.B.M., L.D.N., R.J.O., S.-Y.P., R.E.P., J.M.P., M.H.P., M.A.P., M.L.S., W.T.S., S.S.-S., T.N.S., A.R.S., K.E.S. The data were analyzed by S.-Y.P., M.J.C., L.D.N., B.R.L., Q.X., R.J.O. S.-Y.P., B.R.L. and R.J.O. wrote the first draft which was edited by R.H.B., M.J.C., L.M.G., L.D.N., D.B.K., J.M.P. 4
6 Figure S1. Immunologic features pre-transplant analyzed by genotype and presence or absence of maternal T-cell engraftment. A substantial proportion of infants with SCID variants typically associated with the presence of B cells (IL2RG, IL7R) nevertheless were classified as B low or B- (Panel A). Similarly some infants with variants typically associated with the presence of NK cells (IL7R, RAG1/2, DCLRE1C) were classified as NK low or NK- (Panel B). Out of the cohort, 152 infants were not assessed for maternal T-cell engraftment, and among the 88 tested, maternal T-cell engraftment was absent in 43 infants. Of the 45 infants with maternal engraftment, 22 (49%) had CD3+ T-cell counts >300/µl (Panel C) yet all but 3 had profoundly impaired proliferative responses to phytohemagglutinin of <10% of the lower limit of normal (Panel D). 5
7 Figure S2. Distribution of age at diagnosis and age at transplant. The age at diagnosis and age at transplant both exhibit a bimodal distribution. 6
8 Figure S3. Naïve CD4+ CD45RA+ T-cell count according to conditioning group. The median naïve CD4+ T cell count (indicated by bars) was higher in 23 patients receiving RIC or MAC compared to 62 patients receiving no conditioning or IS (p). 7
9 Table S1: Conditioning regimens Category Total Regimen Number None 120 None 120 Immunosuppression 39 ATG 9 Fludarabine/ATG 7 Alemtuzumab 6 Fludarabine 5 Cyclophosphamide/ATG 5 Fludarabine/alemtuzumab 4 Cyclophosphamide/fludarabine/ATG 1 Cyclophosphamide 1 ATG/alemtuzumab 1 Reduced intensity 35 Busulfan/fludarabine ATG Alemtuzumab None Fludarabine/melphalan ATG Alemtuzumab None Busulfan/cyclophosphamide ATG None Fludarabine/TBI ( cgy) ATG None Fludarabine/alemtuzumab/anti-CD45 2 Busulfan/cyclophosphamide/fludarabine 1 Cyclophosphamide/TBI 1 Fludarabine/cyclophosphamide/TBI 3 TBI 200 cgy 1 Myeloablative 46 Busulfan/cyclophosphamide ATG Alemtuzumab None Busulfan ATG Alemtuzumab Busulfan/fludarabine/ATG 5 Busulfan/cyclophosphamide/fludarabine/ATG Table note: ATG, anti-thymocyte globulin. TBI, total body irradiation. 8
10 Table S2: Patient characteristics Characteristic N % Genotype IL2RG IL7R 22 9 JAK ADA 14 6 PNP 1 0 RAG1/RAG DCLRE1C 11 5 CD3D 2 1 CD3Z 1 0 CD Unknown Age at diagnosis (days), median ( ) (range), n=240 Age at transplant (days), median ( ) (range), n=240 Maternal engraftment Present Absent Not tested Time from diagnosis to transplant, days, median (range) Matched sibling 31.0 ( ) p Mismatched related 34.0 ( ) Other related 28.5 ( ) Unrelated UCB 39.0 ( ) Unrelated PB or BM 88.0 ( ) 9
11 Table S3: Factors associated with age at transplant Variable N months >3.5 months p value n=68 n=172 Family history Yes No Unknown Infection at treatment Diagnosed and not cleared Diagnosed and cleared None Respiratory infection Yes No DNA viral infection Yes No CMV infection Yes No Failure to thrive Yes No Table S4: Probabilities of graft failure by donor type and genotype Factor/Level Total # of 5 yr probability p-value n events (95% CI) Donor type Matched sibling (0-14) Mismatched related (17-31) UCB (6-26) Other related/unrelated BM/PB (5-31) Genotype IL2RG (5-18) ADA (1-28) JAK3/IL7R (12-41) RAG1/2/DCLRE (5-30) Table note: UCB, umbilical cord blood. BM, bone marrow. PB, peripheral blood. 10
12 Table S5: Incidence of GVHD by donor type Donor type N Acute GVHD grade 2-4 at P value 100 days, estimated % (CI) Matched sibling (10-38) 0.058~ Mismatched related (14-28) Mismatched related, (6-22) soybean agglutinin and E rosette depletion Mismatched related, (18-44) CD34 selection Mismatched related, (8-46) other Other matched (10-28) related/unrelated Other matched 26 8 (1-21) related/unrelated, BM or PB Umbilical cord blood (12-38) Donor type N Acute GVHD grade 3-4 at P value 100 days, estimated % (CI) Matched sibling 32 3 (0-14) Mismatched related (6-16) Mismatched related, 69 6 (2-13) soybean agglutinin and E rosette depletion Mismatched related, (7-27) CD34 selection Mismatched related, (2-30) other Other matched 68 6 (2-13) related/unrelated Other matched 26 0 related/unrelated, BM or PB Umbilical cord blood (3-21) Donor type N Chronic GVHD at 2 P value years, estimated % (CI) Matched sibling 32 6 (1-18) 0.040* Mismatched related (10-24) Mismatched related, soybean agglutinin and E 70 9 (4-18) 11
13 rosette depletion Mismatched related, (11-38) CD34 selection Mismatched related, (11-60) other Other matched (8-27) related/unrelated Other matched 25 5 (0-21) related/unrelated, BM or PB Umbilical cord blood (10-35) Table note: GVHD, graft versus host disease. BM, bone marrow. PB, peripheral blood. ~Overall (5 degree of freedom) logrank test comparing all subsets: matched sibling donor versus mismatched related/lectin versus mismatched related/cd34 selection versus mismatched related/other versus other matched related/unrelated donor versus umbilical cord blood. * There is no significant difference in chronic GVHD after omitting the small (n=17) mismatched related, other group (p=0.142). Table S6: Causes of death after transplant Cause of death N (%) None (%) IS (%) RIC (%) MAC (%) Infection 24 (39) 12 (50) 4 (31) 7 (63) 1 (7) Pulmonary 23 (37) 8 (33) 5 (38) 1 (9) 9 (64) Acute GVHD 3 (5) 1 (4) 1 (8) 0 1 (7) Chronic GVHD 1 (2) 1 (4) 0 (0) 0 0 (0) Graft rejection or failure 1 (2) 0 (0) 0 (0) 1 (9) 0 (0) Other organ toxicity 8 (13) 2 (8) 2 (15) 1 (9) 3 (21) Unknown 2 (3) 0 (0) 1 (8) 1 (9) Total 62 (100) 24 (100) 13 (100) 11 (100) Table note: IS, immunosuppression. RIC, reduced intensity conditioning. MAC, myeloablative conditioning. 0 (0) 14 (100) 12
14 Table S7: Multivariate analysis of immune reconstitution Outcome/Outcome Factor Total n # 5 yr OS,% Hazard ratio p value events (95% CI) (CI) Survival Age at transplant and 240 infectious status months (85-98) 1.00 >3.5 months active infection (39-61) ( ) >3.5 months infection resolved (70-90) ( ) >3.5 months no infection (67-98) ( ) >3.5 months, active infection versus no infection ( ) >3.5 months, active infection 3.78 versus infection resolved ( ) >3.5 months, infection resolved versus no infection ( ) Donor type/ conditioning Matched sibling (79-100) 1.00 Mismatched related, no (69-87) conditioning ( ) Mismatched related, with (51-77) conditioning ( ) Umbilical cord blood (40-72) ( ) Other related/unrelated (53-87) 14.2 ( ) Mismatched related, no conditioning vs. with conditioning ( ) Mismatched related, no conditioning vs. umbilical cord blood ( ) Mismatched related, no conditioning vs. Other related/unrelated ( ) Mismatched related, with conditioning vs. umbilical cord blood ( ) Mismatched related, with conditioning vs. other related/unrelated ( ) Umbilical cord blood vs. Other related/unrelated 0.92 ( ) CD3+ T-cell >1000/ul at 2-5 years Total n # events % (95% CI) Odds Ratio (CI) Donor type Matched sibling (55-91) 1.00 Mismatched related (53-77) ( ) Other related/unrelated (58-89) 0.15 ( )
15 Mismatched related versus Other ( ) Conditioning None or immunosuppression (51-73) 1.00 Reduced intensity or (75-97) myeloablative ( ) B cell phenotype B or low (33-63) 1.00 B (76-94) 7.82 ( ) NK cell phenotype NK- or low (73-92) 1.00 NK (42-71) ( ) CD4+ T-cell >500/ul at 2-5 years* Donor type Matched sibling (28-68) 1.00 Mismatched related (19-42) ( ) Other related/unrelated (34-69) ( ) Mismatched related vs. Other ( ) B cell phenotype B- or B low (7-30) 1.00 B (42-66) 8.50 ( ) Off intravenous immunoglobulin replacement at 2-5 years Donor type Matched sibling (61-93) 1.00 Mismatched related (26-49) 0.10 ( ) Other related/unrelated (53-84) ( ) Mismatched related vs. Other ( ) Conditioning None or immunosuppression (31-52) 1.00 Reduced intensity or (69-93) 8.87 myeloablative ( ) Recovery of normal IgA Donor type Matched sibling (78-100) 1.00 Mismatched related (22-47) 0.02 ( ) Other related/unrelated (53-86) 0.05 ( )
16 Mismatched related vs. Other 0.35 ( ) Conditioning None or immunosuppression (35-57) 1.00 Reduced intensity or (65-93) myeloablative ( ) B cell phenotype B- or B low (52-83) 1.00 B (35-59) 0.20 ( ) * In univariate analysis, RAG1/2 and DCLRE1C and ADA deficient SCID were associated with a lower probability of CD4 + T cell recovery (2/14, 0/4 CD4 recovery respectively versus 32/57 IL2RG, p=0.0003). Infection did not reach significance (p=0.093). 15
17 Table S8: Association of full or mixed donor chimerism with various factors Whole blood* B cell Myeloid cell Variable Full Mixed p value Full Mixed Host p value Full Mixed Host p value Donor type Matched sibling Mismatched related Other related/unrelated Conditioning None/IS RIC/MAC Conditioning (no MSD) None/IS RIC/MAC Off intravenous immunoglobulin replacement at 2-5 years On IVIG Off IVIG Genotype IL2RG JAK3/IL7R RAG1/2/DCLRE1C ADA Other/Unknown Table note: MSD, matched sibling donor. IS, immunosuppression. RIC, reduced intensity conditioning. MAC, myeloablative conditioning. IVIG, intravenous immunoglobulin. *All patients had donor T cell engraftment; therefore no patient was fully host, and whole blood chimerism results were either full donor or mixed donor. 16
18 Reference 1 Shearer WT, Dunn E, Notarangelo LD, et al. Establishing Diagnostic Criteria for SCID, Leaky SCID, and OMENN Syndrome: the Primary Immune Deficiency Treatment Consortium Experience. The Journal of allergy and clinical immunology 2013 Nov 27. pii: S (13) doi: /j.jaci [Epub ahead of print] 17
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