Safety and efficacy of narsoplimab in pediatric and adult patients with transplant-associated thrombotic microangiopathy: a real-world experience.


Journal

Bone marrow transplantation
ISSN: 1476-5365
Titre abrégé: Bone Marrow Transplant
Pays: England
ID NLM: 8702459

Informations de publication

Date de publication:
21 May 2024
Historique:
received: 27 02 2024
accepted: 30 04 2024
revised: 29 04 2024
medline: 22 5 2024
pubmed: 22 5 2024
entrez: 21 5 2024
Statut: aheadofprint

Résumé

Transplant-associated thrombotic microangiopathy (TA-TMA) is a severe complication following hematopoietic stem cell transplantation (HSCT). No approved treatments are currently available. This study presents real-world data obtained with narsoplimab, a human immunoglobulin G4 monoclonal antibody that inhibits MASP-2, the effector enzyme of the lectin pathway of the complement system. Between January 2018 and August 2023, 20 (13 adult and 7 pediatric) patients diagnosed with TA-TMA received narsoplimab under an ongoing compassionate use program. The diagnosis was based on internationally defined criteria for pediatric and adult patients. Fifteen patients fulfilled the criteria recently established by an international consensus on TA-TMA. Nineteen patients exhibited high-risk characteristics. Thirteen patients (65%) responded to narsoplimab, achieving transfusion independence and significant clinical improvement. The one-hundred-day Overall Survival (OS) post-TA-TMA diagnosis was 70%, and 100% for responders. Narsoplimab proved to be effective and safe in the treatment of high-risk TA-TMA, with no increased infectious complications or other safety signals of concern across all age groups. The high response rates and the encouraging survival outcomes underscore the potential of narsoplimab as a valuable therapeutic option, particularly for high-risk cases.

Identifiants

pubmed: 38773280
doi: 10.1038/s41409-024-02305-3
pii: 10.1038/s41409-024-02305-3
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

© 2024. The Author(s).

Références

Jodele S, Davies SM, Lane A, Khoury J, Dandoy C, Goebel J, et al. Diagnostic and risk criteria for HSCT-associated thrombotic microangiopathy: a study in children and young adults. 2014;124:645–53
Gavriilaki E, Ho VT, Schwaeble W, Dudler T, Daha M, Fujita T, et al. Role of the lectin pathway of complement in hematopoietic stem cell transplantation-associated endothelial injury and thrombotic microangiopathy. Exp Hematol Oncol. 2021;10. https://doi.org/10.1186/s40164-021-00249-8
Schoettler M, Lehmann L, Li A, Ma C, Duncan C. Thrombotic microangiopathy following pediatric autologous hematopoietic cell transplantation: a report of significant end-organ dysfunction in eculizumab-treated survivors. Biol Blood Marrow Transplant. 2019;25:e163–8. https://doi.org/10.1016/j.bbmt.2018.12.840 .
doi: 10.1016/j.bbmt.2018.12.840 pubmed: 30639820 pmcid: 6822269
Ho VT, Cutler C, Carter S, Martin P, Adams R, Horowitz M, et al. Blood and marrow transplant clinical trials network toxicity committee consensus summary: thrombotic microangiopathy after hematopoietic stem cell transplantation. Biol Blood Marrow Transplant. 2005;11:571–5.
doi: 10.1016/j.bbmt.2005.06.001 pubmed: 16041306
Ruutu T, Barosi G, Benjamin RJ, Clark RE, George JN, Gratwohl A, et al. Diagnostic criteria for hematopoietic stem cell transplant-associated microangiopathy: results of a consensus process by an International Working Group. Haematologica. 2007;92:95–100.
doi: 10.3324/haematol.10699 pubmed: 17229640
Cho BS, Yahng SA, Lee SE, Eom KS, Kim YJ, Kim HJ, et al. Validation of recently proposed consensus criteria for thrombotic microangiopathy after allogeneic hematopoietic stem-cell transplantation. Transplantation. 2010;90:918–26.
doi: 10.1097/TP.0b013e3181f24e8d pubmed: 20717073
Schoettler ML, Carreras E, Cho B, Dandoy CE, Ho VT, Jodele S, et al. Harmonizing definitions for diagnostic criteria and prognostic assessment of transplantation-associated thrombotic microangiopathy: a report on behalf of the European Society for Blood and Marrow Transplantation, American Society for Transplantation and C. Transplant Cell Ther. 2023;29:151–63.
doi: 10.1016/j.jtct.2022.11.015 pubmed: 36442770
Yang J, Xu X, Han S, Qi J, Li X, Pan T, et al. Comparison of multiple treatments in the management of transplant-related thrombotic microangiopathy: a network meta-analysis. Ann Hematol. 2023;102:31–9. https://doi.org/10.1007/s00277-022-05069-2 .
doi: 10.1007/s00277-022-05069-2 pubmed: 36547721
Rotz SJ, Dandoy CE, Davies SM. ST2 and endothelial injury as a link between GVHD and microangiopathy. N Engl J Med. 2017;376:1189–90.
doi: 10.1056/NEJMc1700185 pubmed: 28328331
Kraft S, Bollinger N, Bodenmann B, Heim D, Bucher C, Lengerke C, et al. High mortality in hematopoietic stem cell transplant-associated thrombotic microangiopathy with and without concomitant acute graft-versus-host disease. Bone Marrow Transplant. 2019;54:540–8. https://doi.org/10.1038/s41409-018-0293-3 .
doi: 10.1038/s41409-018-0293-3 pubmed: 30108323
Pagliuca S, Michonneau D, De Fontbrune FS, Del Galy AS, Xhaard A, Robin M, et al. Allogeneic reactivity-mediated endothelial cell complications after HSCT: a plea for consensual definitions. Blood Adv. 2019;3:2424–35.
doi: 10.1182/bloodadvances.2019000143 pubmed: 31409584 pmcid: 6693000
Young JA, Pallas CR, Knovich MA. Transplant-associated thrombotic microangiopathy: theoretical considerations and a practical approach to an unrefined diagnosis. Bone Marrow Transplant. 2021;56:1805–17. https://doi.org/10.1038/s41409-021-01283-0 .
doi: 10.1038/s41409-021-01283-0 pubmed: 33875812 pmcid: 8338557
Dhakal P, Giri S, Pathak R, Bhatt VR. Eculizumab in transplant-associated thrombotic microangiopathy. Clin Appl Thromb. 2017;23:175–80.
doi: 10.1177/1076029615599439
Yeates L, Slatter MA, Bonanomi S, Lim FLWI, Ong SY, Dalissier A, et al. Use of defibrotide to treat transplant-associated thrombotic microangiopathy: a retrospective study of the paediatric diseases and inborn errors working parties of the European Society of Blood and Marrow Transplantation. Bone Marrow Transplant. 2017;52:762–4.
doi: 10.1038/bmt.2016.351 pubmed: 28092354
Jodele S, Sabulski A. Reeling in complement in transplant‐associated thrombotic microangiopathy: you’re going to need a bigger boat. Am J Hematol. 2023;98:57–73.
doi: 10.1002/ajh.26872
Jodele S. Complement in pathophysiology and treatment of transplant-associated thrombotic microangiopathies. Semin Hematol. 2018;55:159–66.
doi: 10.1053/j.seminhematol.2018.04.003 pubmed: 30032753
Ardissino G, Salardi S, Berra S, Colussi G, Cugno M, Zecca M, et al. Acquired complement regulatory gene mutations and hematopoietic stem cell transplant–related thrombotic microangiopathy. Biol Blood Marrow Transplant. 2017;23:1580–2. https://doi.org/10.1016/j.bbmt.2017.05.013
doi: 10.1016/j.bbmt.2017.05.013 pubmed: 28522344
West EE, Woodruff T, Fremeaux-Bacchi V, Kemper C. Complement in human disease: approved and up-and-coming therapeutics. Lancet. 2023;403:392–405. https://doi.org/10.1016/S0140-6736(23)01524-6 .
doi: 10.1016/S0140-6736(23)01524-6 pubmed: 37979593 pmcid: 10872502
Jodele S, Fukuda T, Mizuno K, Vinks AA, Laskin BL, Goebel J, et al. Variable eculizumab clearance requires pharmacodynamic monitoring to optimize therapy for thrombotic microangiopathy after hematopoietic stem cell transplantation. Biol Blood Marrow Transplant. 2016;22:307–15.
doi: 10.1016/j.bbmt.2015.10.002 pubmed: 26456258
Bohl SR, Kuchenbauer F, von Harsdorf S, Kloevekorn N, Schönsteiner SS, Rouhi A, et al. Thrombotic microangiopathy after allogeneic stem cell transplantation: a comparison of eculizumab therapy and conventional therapy. Biol Blood Marrow Transplant. 2017;23:2172–7. https://doi.org/10.1016/j.bbmt.2017.08.019 .
doi: 10.1016/j.bbmt.2017.08.019 pubmed: 28860002
Elhadad S, Chapin J, Copertino D, Van Besien K, Ahamed J, Laurence J. MASP2 levels are elevated in thrombotic microangiopathies: association with microvascular endothelial cell injury and suppression by anti-MASP2 antibody narsoplimab. Clin Exp Immunol. 2021;203:96–104.
doi: 10.1111/cei.13497 pubmed: 32681658
Rambaldi A, Gritti G, Micò MC, Frigeni M, Borleri G, Salvi A, et al. Endothelial injury and thrombotic microangiopathy in COVID-19: treatment with the lectin-pathway inhibitor narsoplimab. Immunobiology. 2020;225:152001.
doi: 10.1016/j.imbio.2020.152001 pubmed: 32943233 pmcid: 7415163
Merle NS, Church SE, Fremeaux-Bacchi V, Roumenina LT. Complement system part I - molecular mechanisms of activation and regulation. Front Immunol. 2015;6:262.
Khaled SK, Claes K, Goh YT, Kwong YL, Leung N, Mendrek W, et al. Narsoplimab, a mannan-binding lectin-associated serine protease-2 inhibitor, for the treatment of adult hematopoietic stem-cell transplantation-associated thrombotic microangiopathy. J Clin Oncol. 2022;40:2447–57.
El-Bietar J, Warren M, Dandoy C, Myers KC, Lane A, Wallace G, et al. Histologic features of intestinal thrombotic microangiopathy in pediatric and young adult patients after hematopoietic stem cell transplantation. Biol Blood Marrow Transplant. 2015;21:1994–2001. https://doi.org/10.1016/j.bbmt.2015.06.016 .
doi: 10.1016/j.bbmt.2015.06.016 pubmed: 26150023 pmcid: 4604068
Warren M, Jodele S, Dandoy C, Myers KC, Wallace G, Nelson A, et al. A complete histologic approach to gastrointestinal biopsy from hematopoietic stem cell transplant patients with evidence of transplant-associated gastrointestinal thrombotic microangiopathy. Arch Pathol Lab Med. 2017;141:1558–66.
doi: 10.5858/arpa.2016-0599-RA pubmed: 28795840
Inamoto Y, Ito M, Suzuki R, Nishida T, Iida H, Kohno A, et al. Clinicopathological manifestations and treatment of intestinal transplant-associated microangiopathy. Bone Marrow Transplant. 2009;44:43–9.
doi: 10.1038/bmt.2008.419 pubmed: 19139727
Wall SA, Zhao Q, Yearsley M, Blower L, Agyeman A, Ranganathan P, et al. Complement-mediated thrombotic microangiopathy as a link between endothelial damage and steroid-refractory GVHD. Blood Adv. 2018;2:2619–28.
doi: 10.1182/bloodadvances.2018020321 pubmed: 30327370 pmcid: 6199668
Nishida T, Hamaguchi M, Hirabayashi N, Haneda M, Terakura S, Atsura Y, et al. Intestinal thrombotic microangiopathy after allogeneic bone marrow transplantation: a clinical imitator of acute enteric graft-versus-host disease. Bone Marrow Transplant. 2004;33:1143–50.
doi: 10.1038/sj.bmt.1704512 pubmed: 15077133
Jodele S, Dandoy CE, Lane A, Laskin BL, Teusink-Cross A, Myers KC, et al. Complement blockade for TA-TMA: Lessons learned from a large pediatric cohort treated with eculizumab. Blood. 2020;135:1049–57.
pubmed: 31932840 pmcid: 7099329
Mizuno K, Dandoy CE, Teusink-Cross A, Davies SM, Vinks AA, Jodele S. Eculizumab precision-dosing algorithm for thrombotic microangiopathy in children and young adults undergoing HSCT. Blood Adv. 2022;6:1454–63. https://doi.org/10.1182/bloodadvances.2021006523 .
doi: 10.1182/bloodadvances.2021006523 pubmed: 35008105 pmcid: 8905690
Rudoni J, Jan A, Hosing C, Aung F, Yeh J. Eculizumab for transplant-associated thrombotic microangiopathy in adult allogeneic stem cell transplant recipients. Eur J Haematol. 2018;101:389–98.
doi: 10.1111/ejh.13127 pubmed: 29920784
Alhomoud M, Scordo M, Perales MA. Successful use of narsoplimab to treat allogeneic transplant-associated thrombotic microangiopathy while maintaining sirolimus. Bone Marrow Transplant. 2024 https://doi.org/10.1038/s41409-024-02263-w .
Matsui H, Arai Y, Imoto H, Mitsuyoshi T, Tamura N, Kondo T, et al. Risk factors and appropriate therapeutic strategies for thrombotic microangiopathy after allogeneic HSCT. Blood Adv. 2020;4:3169–79.
doi: 10.1182/bloodadvances.2020002007 pubmed: 32658984 pmcid: 7362379
Jodele S, Davies SM, Lane A, Khoury J, Dandoy C, Goebel J, et al. Diagnostic and risk criteria for HSCT-associated thrombotic microangiopathy: a study in children and young adults. Blood. 2014;124:645–53.
doi: 10.1182/blood-2014-03-564997 pubmed: 24876561 pmcid: 4110664
Gavriilaki E, Sakellari I, Chatzikonstantinou T, Mallouri D, Batsis I, Vardi A, et al. Endothelial and complement activation as predictors of survival in adult allogeneic hematopoietic cell transplantation. HemaSphere. 2021;5:E487.
doi: 10.1097/HS9.0000000000000487 pubmed: 33324949
Schoettler M, Lehmann LE, Margossian S, Lee M, Kean LS, Kao PC, et al. Risk factors for transplant-associated thrombotic microangiopathy and mortality in a pediatric cohort. Blood Adv. 2020;4:2536–47.
doi: 10.1182/bloodadvances.2019001242 pubmed: 32516415 pmcid: 7284101

Auteurs

Marta Castelli (M)

Department of Oncology and Hematology, University of Milan and Azienda Socio-Sanitaria Territoriale Papa Giovanni XXIII, Bergamo, Italy.

Maria Caterina Micò (MC)

Department of Oncology and Hematology, Azienda Socio-Sanitaria Territoriale Papa Giovanni XXIII, Bergamo, Italy.

Anna Grassi (A)

Department of Oncology and Hematology, Azienda Socio-Sanitaria Territoriale Papa Giovanni XXIII, Bergamo, Italy.

Alessandra Algarotti (A)

Department of Oncology and Hematology, Azienda Socio-Sanitaria Territoriale Papa Giovanni XXIII, Bergamo, Italy.

Federico Lussana (F)

Department of Oncology and Hematology, University of Milan and Azienda Socio-Sanitaria Territoriale Papa Giovanni XXIII, Bergamo, Italy.
Department of Oncology and Hematology, Azienda Socio-Sanitaria Territoriale Papa Giovanni XXIII, Bergamo, Italy.

Maria Chiara Finazzi (MC)

Department of Oncology and Hematology, Azienda Socio-Sanitaria Territoriale Papa Giovanni XXIII, Bergamo, Italy.

Benedetta Rambaldi (B)

Department of Oncology and Hematology, Azienda Socio-Sanitaria Territoriale Papa Giovanni XXIII, Bergamo, Italy.

Chiara Pavoni (C)

Department of Oncology and Hematology, Azienda Socio-Sanitaria Territoriale Papa Giovanni XXIII, Bergamo, Italy.

Giuliana Rizzuto (G)

Department of Oncology and Hematology, Azienda Socio-Sanitaria Territoriale Papa Giovanni XXIII, Bergamo, Italy.

Paola Tebaldi (P)

Department of Pathology, Azienda Socio-Sanitaria Territoriale Papa Giovanni XXIII, Bergamo, Italy.

Francesca Vendemini (F)

Department of Pediatrics, Fondazione IRCCS San Gerardo, Monza, Italy.

Marta Verna (M)

Department of Pediatrics, Fondazione IRCCS San Gerardo, Monza, Italy.

Sonia Bonanomi (S)

Department of Pediatrics, Fondazione IRCCS San Gerardo, Monza, Italy.

Andrea Biondi (A)

Department of Pediatrics, Fondazione IRCCS San Gerardo, Monza, Italy.
Department of Medicine and Surgery, University of Milano-Bicocca, Monza, Italy.

Adriana Balduzzi (A)

Department of Pediatrics, Fondazione IRCCS San Gerardo, Monza, Italy.
Department of Medicine and Surgery, University of Milano-Bicocca, Monza, Italy.

Alessandro Rambaldi (A)

Department of Oncology and Hematology, University of Milan and Azienda Socio-Sanitaria Territoriale Papa Giovanni XXIII, Bergamo, Italy. alessandro.rambaldi@unimi.it.
Department of Oncology and Hematology, Azienda Socio-Sanitaria Territoriale Papa Giovanni XXIII, Bergamo, Italy. alessandro.rambaldi@unimi.it.

Giacomo Gotti (G)

Department of Pediatrics, Fondazione IRCCS San Gerardo, Monza, Italy.

Classifications MeSH