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The Effect of NIMA Matching in Adult Unrelated Mismatched

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Bone Marrow Transplantation (2019) 54:849–857 https://doi.org/10.1038/s41409-018-0345-8 ARTICLE The effect of NIMA matching in adult unrelated mismatched hematopoietic stem cell transplantation – a joint study of the Acute Leukemia Working Party of the EBMT and the CIBMTR 1 2,3 1 1 4 Julia Pingel ● Tao Wang ● Yvonne Hagenlocher ● Camila J. Hernández-Frederick ● Arnon Nagler ● 5 6 7 8 2,9 Michael D. Haagenson ● Katharina Fleischhauer ● Katharine C. Hsu ● Michael R. Verneris ● Stephanie J. Lee ● 10 11 5 1 12,13 Mohamad Mohty ● Emmanuelle Polge ● Stephen R. Spellman ● Alexander H. Schmidt ● Jon J. van Rood Received: 12 June 2018 / Revised: 10 August 2018 / Accepted: 30 August 2018 / Published online: 2 October 2018 © Springer Nature Limited 2018 Abstract Hematological malignancies can be cured by unrelated donor allogeneic HSCT and outcomes are optimized by high- resolution HLA matching at HLA-A, -B, -C, -DRB1 and -DQB1 (10/10 match). If a 10/10 match is unavailable, 9/10 matches may be suitable. Fetal exposure to non-inherited maternal antigens (NIMA) may impart lifelong NIMA tolerance modulating the immune response, as shown in adult haploidentical transplantation. In cord blood transplantation, NIMA 1234567890();,: 1234567890();,: matching lowered rates of aGvHD and TRM; in haploidentical transplantation, sibling donors with non-shared maternal antigens showed less grade II-IV aGvHD. This retrospective analysis examined if 9/10 matched unrelated donor HSCT benefits from NIMA matching. DKMS contacted 1,735 donors and obtained 733 (42%) maternal samples. NIMA-matched and -mismatched cases with a minimum follow-up of 1 year were compared by univariate and multivariate analyses adjusted for co-variates for OS, DFS, relapse, TRM and a/cGvHD. The study population (N = 445) comprised 31 NIMA-matched and 414 NIMA-mismatched cases. No significant differences between NIMA-matched and NIMA-mismatched groups were found for any outcomes with similar OS and TRM rates within both groups. This study provides the proof of principle that NIMA matching is possible in the unrelated donor HSCT setting; larger studies may be able to provide significant results. Introduction Matching of human leukocyte antigen (HLA) genes is critical for optimizing transplant outcomes, including sur- Allogeneic hematopoietic stem cell transplantation (HSCT) vival [1–3]. However, only about 30% of transplant offers a potential curative therapy for a variety of hemato- patients have an HLA-identical sibling donor, leaving logical malignancies and other diseases of the blood. 70% in need of an alternative source of stem cells from * Stephen R. Spellman 7 Memorial Sloan Kettering Cancer Center, New York, NY, USA [email protected] 8 University of Colorado - Children’s Hospital, Aurora, CO, USA 1 DKMS, Tübingen, Germany 9 Clinical Research Division, Fred Hutchinson Cancer Research 2 Center for International Blood and Marrow Transplant Research, Center, Seattle, WA, USA Medical College of Wisconsin, Milwaukee, WI, USA 10 Department of Haemotology, Saint Antoine Hospital, 3 Division of Biostatistics, Institute for Health and Society, Medical Paris, France College of Wisconsin, Milwaukee, WI, USA 11 EBMT (European Society for Blood and Marrow Transplantation), 4 Sheba Medical Center, Sheba Cord Blood Bank, Tel- Department of Haematology, Saint Antoine Hospital, Université Hashomer, Israel Pierre et Marie Curie, INSERM UMR 938, Paris, France 5 Center for International Blood and Marrow Transplant Research, 12 Matchis Foundation, Leiden, The Netherlands Minneapolis, MN, USA 13 Department of Immunohematology and Blood Transfusion, 6 Institute for Experimental Cellular Therapy, University Hospital Leiden University Medical Centre, Leiden, The Netherlands Essen, Essen, Germany 850 J. Pingel et al. an unrelated donor, a haploidentical donor or a cord blood T-cell-depleted HSCT with HLA-haploidentical donors unit [4, 5]. If a fully HLA-A, -B, -C, -DRB1 and -DQB1 risk for acute GvHD (aGvHD) grade II-IV was reduced (10/10) matched unrelated donor is unavailable, 9/10 when the sibling donor shared the paternal haplotype but matched donors may be an acceptable alternative and can be not the maternal one, as found before in kidney trans- found at high frequency in stem cell donor registries [5]. plantation [18, 19]. However, van Rood et al. showed that High- and low-risk HLA allele mismatches for severe graft- haploidentical sibling transplantation with no shared versus-host disease (GvHD) have been described [6]. maternal antigens had similar graft failure rates and sur- However, the prioritization and identification of permissive vival, while TRM was reduced for sibling donors com- or acceptable HLA mismatches in the mismatched paredtoparentaldonors[18]. setting have proven elusive for HLA-A, -B, -C, -DRB1 and Because of the general unavailability of maternal HLA -DQB1 [7–9]. typing, no studies to date have analyzed the NIMA effect in During pregnancy, the fetus and mother gain tolerance to the unrelated adult donor HSCT setting. This joint European each other’s alloantigens [10]. It has been shown that Society for Blood and Marrow Transplantation (EBMT)- exposure to non-inherited maternal antigens (NIMAs) dur- Center for International Blood and Marrow Transplant ing in utero development or even only during breastfeeding Research (CIBMTR) retrospective study was specifically can impart lifelong immunomodulating effects and long- designed to study the effect of NIMAs on the outcome of lasting tolerance against specific NIMAs—the so-called adult unrelated mismatched HSCT. A verification of the NIMA effect [7, 10, 11]. In mismatched unrelated HSCT, if benefit in outcome by NIMA matching could have a con- the recipient and the donor’s mother share the NIMA for the siderable impact on donor search and selection by routinely mismatched HLA locus, the case is considered a NIMA requesting a maternal sample during confirmatory typing match. However, the existence of this NIMA effect, espe- and using NIMA matching as a criterion for mismatched cially for the outcome of adult unrelated allogeneic HSCT, donor selection. is still under scientific debate [12, 13]. Prior solid organ transplantation studies revealed tol- erance to NIMAs suggesting that the patient’s immune Materials and methods system does not recognize these antigens as foreign. Although maternal kidney allografts did not show a better Study population survival compared to paternal ones [12], another study on kidney grafts showed a superior 5- and 10-year post- Patients eligible for this study received a T-cell-replete transplantation survival when donated by haploidentical mismatched unrelated bone marrow or peripheral blood siblings with a matched paternal haplotype and differing stem cell transplant for acute myeloid leukemia (AML) or maternal haplotype compared to haploidentical siblings acute lymphoblastic leukemia (ALL) between 1999 and sharing the maternal haplotype and not the paternal one 2013. Further eligibility criteria were the following: (1) all [14]. This result was consistent with a study showing that donors were listed with the German donor center DKMS; kidney transplants with a mismatched HLA-A antigen (2) recipient-donor pairs’ outcome data were recorded identical to the patient’s NIMA had superior long-term with a minimum 1 year follow-up at the EBMT or the graft survival [15]. In umbilical cord blood transplantation CIBMTR; (3) recipient-donor pairs had exactly one HLA (UCBT), transplant-related mortality (TRM) at 5 years mismatch at HLA-A, -B, -C, -DRB1 or -DQB1; (4) DNA post transplantation was reduced after NIMA-matched sample from donor’s mother could be obtained for high- compared to NIMA-mismatched transplantation, 18% resolution HLA typing of the mismatched locus. versus 32%, respectively [16]. Overall survival (OS) was Recipient-donor pairs fulfilling the inclusion criteria were also increased after NIMA-matched UCBT [16]. An ana- selected from EBMT and CIBMTR databases. Cases lysis by van Rood et al. found that NIMA matches in where the patient received a second HSCT were censored UCBT between a recipient and an unrelated donor in at the time of second transplantation. Information about HLA-A,-Bor-DRB1resultedinreducedTRM,overall the donor mother’s HLA typing results were not available mortality and treatment failure and was attributed to a at the start of the study. The institutional review board of faster neutrophil recovery [7]. In contrast, another report the Technische Universität Dresden (IRB00001473) showed no association between NIMA-matched UCBTs approved the study design that included contacting the and TRM or overall mortality [17]. For HSCT, comparing donor’s mother. For maternal DNA sample retrieval, durable engraftment with organ allograft survival, it could DKMS prepared a sendout package to the donors con- be expected that there should be less GvHD and conse- taining study information material, an informed consent quently superior transplantation success if the mismatched form and a buccal swab kit for sample collection to be donor is NIMA-matched to the patient. In studies of non- sent on to the donors’ mothers. The effect of NIMA matching in adult unrelated mismatched hematopoietic stem cell transplantation – a. 851 HLA typing and match assignment -mismatched groups. All clinical variables were tested for affirmation of the proportional hazards assumption. Factors DNA samples of donors and donors’ mothers were HLA- violating the proportional hazards assumption were adjusted typed at high
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