The MAGIC algorithm probability predicts treatment response and long-term outcomes to second-line therapy for acute GVHD

Author:

DeFilipp Zachariah1ORCID,Kim Haesook T.2,Spyrou Nikolaos3,Katsivelos Nikolaos3ORCID,Kowalyk Steven3,Eng Gilbert3,Kasikis Stelios3,Beheshti Rahnuma3,Baez Janna3,Akahoshi Yu3ORCID,Ayuk Francis4,Choe Hannah5,Etra Aaron3,Grupp Stephan A.6,Hexner Elizabeth O.7ORCID,Hogan William J.8ORCID,Kitko Carrie L.9,Qayed Muna10ORCID,Reshef Ran11ORCID,Vasova Ingrid12,Zeiser Robert13,Young Rachel3,Holler Ernst14,Ferrara James L. M.3,Nakamura Ryotaro15ORCID,Levine John E.3ORCID,Chen Yi-Bin1ORCID

Affiliation:

1. 1Hematopoietic Cell Transplant and Cellular Therapy Program, Massachusetts General Hospital, Boston, MA

2. 2Department of Data Science, Dana-Farber Cancer Institute and Harvard T.H. Chan School of Public Health, Boston, MA

3. 3The Tisch Cancer Institute, Icahn School of Medicine at Mount Sinai, New York, NY

4. 4Department of Stem Cell Transplantation, University Medical Center Hamburg-Eppendorf, Hamburg, Germany

5. 5Division of Hematology, James Cancer Center, The Ohio State University, Columbus, OH

6. 6Division of Oncology, Children’s Hospital of Philadelphia, Philadelphia, PA

7. 7Blood and Marrow Transplantation Program, Abramson Cancer Center, Perelman School of Medicine at the University of Pennsylvania, Philadelphia, PA

8. 8Division of Hematology, Mayo Clinic, Rochester, MN

9. 9Pediatric Stem Cell Transplant Program, Vanderbilt University Medical Center, Nashville, TN

10. 10Aflac Cancer and Blood Disorders Center, Emory University, Atlanta, GA

11. 11Blood and Marrow Transplantation Program, Columbia University Medical Center, New York, NY

12. 12Department of Internal Medicine 5, Hematology/Oncology, University Hospital Erlangen, Erlangen, Germany

13. 13Department of Medicine I - Medical Centre, Faculty of Medicine, University of Freiburg, Freiburg, Germany

14. 14Department of Hematology and Oncology, Internal Medicine III, University of Regensburg, Regensburg, Germany

15. 15Hematology/Hematopoietic Cell Transplant, City of Hope National Medical Center, Duarte, CA

Abstract

Abstract The significance of biomarkers in second-line treatment for acute graft-versus-host disease (GVHD) has not been well characterized. We analyzed clinical data and serum samples at the initiation of second-line systemic treatment of acute GVHD from 167 patients from 17 centers of the Mount Sinai Acute GVHD International Consortium (MAGIC) between 2016 and 2021. Sixty-two patients received ruxolitinib-based therapy, whereas 102 received other systemic agents. In agreement with prospective trials, ruxolitinib resulted in a higher day 28 (D28) overall response Frate than nonruxolitinib therapies (55% vs 31%, P = .003) and patients who received ruxolitinib had significantly lower nonrelapse mortality (NRM) than those who received nonruxolitinib therapies (point estimates at 2-year: 35% vs 61%, P = .002). Biomarker analyses demonstrated that the benefit from ruxolitinib was observed only in patients with low MAGIC algorithm probabilities (MAPs) at the start of second-line treatment. Among patients with a low MAP, those who received ruxolitinib experienced significantly lower NRM than those who received nonruxolitinib therapies (point estimates at 2-year: 12% vs 41%, P = .016). However, patients with high MAP experienced high NRM regardless of treatment with ruxolitinib or nonruxolitinib therapies (point estimates at 2-year: 67% vs 80%, P = .65). A landmark analysis demonstrated that the relationship between the D28 response and NRM largely depends on the MAP level at the initiation of second-line therapy. In conclusion, MAP measured at second-line systemic treatment for acute GVHD predicts treatment response and NRM. The outcomes of patients with high MAP are poor regardless of treatment choice, and ruxolitinib appears to primarily benefit patients with low MAP.

Publisher

American Society of Hematology

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