Inotuzumab Ozogamicin for Relapsed/Refractory Acute Lymphoblastic Leukemia in the INO-VATE Trial: CD22 Pharmacodynamics, Efficacy, and Safety by Baseline CD22.
Antineoplastic Agents, Immunological
/ administration & dosage
Disease Management
Disease Susceptibility
Drug Resistance, Neoplasm
Humans
Inotuzumab Ozogamicin
/ administration & dosage
Precursor Cell Lymphoblastic Leukemia-Lymphoma
/ drug therapy
Recurrence
Retreatment
Sialic Acid Binding Ig-like Lectin 2
/ metabolism
Treatment Outcome
Journal
Clinical cancer research : an official journal of the American Association for Cancer Research
ISSN: 1557-3265
Titre abrégé: Clin Cancer Res
Pays: United States
ID NLM: 9502500
Informations de publication
Date de publication:
15 05 2021
15 05 2021
Historique:
received:
21
06
2020
revised:
03
12
2020
accepted:
10
02
2021
pubmed:
20
2
2021
medline:
17
3
2022
entrez:
19
2
2021
Statut:
ppublish
Résumé
We assessed the relationship between cluster of differentiation-22 (CD22) expression and outcomes of inotuzumab ozogamicin versus standard of care (SC) in INO-VATE (NCT01564784). Adults with relapsed/refractory B-cell precursor CD22-positive (by local or central laboratory) acute lymphoblastic leukemia were randomized to inotuzumab ozogamicin ( Most patients had high (≥90%) CD22 positivity per central laboratory. The response rate was significantly higher with inotuzumab ozogamicin versus SC. Minimal/measurable residual disease negativity, duration of remission (DoR), progression-free survival, and overall survival (OS) were significantly better with inotuzumab ozogamicin versus SC in patients with CD22 positivity ≥90%. Fewer patients had CD22 positivity <90%; for whom, response rates were higher with inotuzumab ozogamicin versus SC, but DoR and OS appeared similar. Similar trends were evident in quartile analyses of CD22 MESF and CD22 positivity per local laboratory. Among inotuzumab ozogamicin-responding patients with subsequent relapse, decrease in CD22 positivity and receptor density was evident, but not the emergence of CD22 negativity. Rates of grade ≥3 hematologic adverse events (AEs) were similar and hepatobiliary AEs rate was higher for inotuzumab ozogamicin versus SC. No apparent relationship was observed between the rates of hematologic and hepatic AEs and CD22 expression. Inotuzumab ozogamicin demonstrated a favorable benefit-risk profile versus SC in patients with higher and lower CD22 expression. Patients with high CD22 expression and normal cytogenetics benefited the most from inotuzumab ozogamicin therapy.
Identifiants
pubmed: 33602684
pii: 1078-0432.CCR-20-2399
doi: 10.1158/1078-0432.CCR-20-2399
doi:
Substances chimiques
Antineoplastic Agents, Immunological
0
CD22 protein, human
0
Sialic Acid Binding Ig-like Lectin 2
0
Inotuzumab Ozogamicin
P93RUU11P7
Banques de données
ClinicalTrials.gov
['NCT01564784']
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
2742-2754Informations de copyright
©2021 American Association for Cancer Research.
Références
Global, regional, and national cancer incidence, mortality, years of life lost, years lived with disability, and disability-adjusted life-years for 29 cancer groups, 1990 to 2017: a systematic analysis for the global burden of disease study. JAMA Oncol. 2019;5:1749–68.
Terwilliger T, Abdul-Hay M. Acute lymphoblastic leukemia: a comprehensive review and 2017 update. Blood Cancer J. 2017;7:e577.
Jabbour E, O'Brien S, Huang X, Thomas D, Rytting M, Sasaki K, et al. Prognostic factors for outcome in patients with refractory and relapsed acute lymphocytic leukemia treated with inotuzumab ozogamicin, a CD22 monoclonal antibody. Am J Hematol. 2015;90:193–6.
Gudowius S, Recker K, Laws HJ, Dirksen U, Troger A, Wieczorek U, et al. Identification of candidate target antigens for antibody-based immunotherapy in childhood B-cell precursor ALL. Klin Padiatr. 2006;218:327–33.
de Vries JF, Zwaan CM, De Bie M, Voerman JS, den Boer ML, van Dongen JJ, et al. The novel calicheamicin-conjugated CD22 antibody inotuzumab ozogamicin (CMC-544) effectively kills primary pediatric acute lymphoblastic leukemia cells. Leukemia. 2012;26:255–64.
Haso W, Lee DW, Shah NN, Stetler-Stevenson M, Yuan CM, Pastan IH, et al. Anti-CD22-chimeric antigen receptors targeting B-cell precursor acute lymphoblastic leukemia. Blood. 2013;121:1165–74.
Shah NN, Stetler-Stevenson M, Yuan CM, Richards K, Delbrook C, Kreitman RJ, et al. Characterization of CD22 expression in acute lymphoblastic leukemia. Pediatr Blood Cancer. 2015;62:964–9.
Jabbour E, O'Brien S, Ravandi F, Kantarjian H. Monoclonal antibodies in acute lymphoblastic leukemia. Blood. 2015;125:4010–6.
Siegel AB, Goldenberg DM, Cesano A, Coleman M, Leonard JP. CD22-directed monoclonal antibody therapy for lymphoma. Semin Oncol. 2003;30:457–64.
Ricart AD. Antibody-drug conjugates of calicheamicin derivative: gemtuzumab ozogamicin and inotuzumab ozogamicin. Clin Cancer Res. 2011;17:6417–27.
Shor B, Gerber HP, Sapra P. Preclinical and clinical development of inotuzumab-ozogamicin in hematological malignancies. Mol Immunol. 2015;67:107–16.
Kantarjian HM, DeAngelo DJ, Stelljes M, Martinelli G, Liedtke M, Stock W, et al. Inotuzumab ozogamicin versus standard therapy for acute lymphoblastic leukemia. N Engl J Med. 2016;375:740–53.
Kantarjian HM, DeAngelo DJ, Stelljes M, Liedtke M, Stock W, Gokbuget N, et al. Inotuzumab ozogamicin versus standard of care in relapsed or refractory acute lymphoblastic leukemia: final report and long-term survival follow-up from the randomized, phase 3 INO-VATE study. Cancer. 2019;125:2474–87.
Moorman AV. New and emerging prognostic and predictive genetic biomarkers in B-cell precursor acute lymphoblastic leukemia. Haematologica. 2016;101:407–16.
Winters AC, Bernt KM. MLL-rearranged leukemias-an update on science and clinical approaches. Front Pediatr. 2017;5:4.
Ruella M, Maus MV. Catch me if you can: leukemia escape after CD19-directed T cell immunotherapies. Comput Struct Biotechnol J. 2016;14:357–62.
Shah NN, O'Brien MM, Yuan C, Ji L, Xu X, Rheingold SR, et al. Evaluation of CD22 modulation as a mechanism of resistance to inotuzumab ozogamicin (InO): results from central CD22 testing on the Children's Oncology Group (COG) phase II trial of INO in children and young adults with CD22+ B-acute lymphoblastic leukemia (B-ALL). J Clin Oncol. 2020;38:10519.
Jabbour E, Gokbuget N, Advani A, Stelljes M, Stock W, Liedtke M, et al. Impact of minimal residual disease status in patients with relapsed/refractory acute lymphoblastic leukemia treated with inotuzumab ozogamicin in the phase III INO-VATE trial. Leuk Res. 2019;88:106283.
Schwartz A, Gaigalas AK, Wang L, Marti GE, Vogt RF, Fernandez-Repollet E. Formalization of the MESF unit of fluorescence intensity. Cytometry B Clin Cytom. 2004;57:1–6.
Jabbour E, O'Brien S, Konopleva M, Kantarjian H. New insights into the pathophysiology and therapy of adult acute lymphoblastic leukemia. Cancer. 2015;121:2517–28.
Hoelzer D, Bassan R, Dombret H, Fielding A, Ribera JM, Buske C, et al. Acute lymphoblastic leukaemia in adult patients: ESMO clinical practice guidelines for diagnosis, treatment and follow-up. Ann Oncol. 2016;27:v69–82.
Brookmeyer R, Crowley J. A confidence interval for the median survival time. Biometrics. 1982;38:29–41.
Garrett M, Ruiz-Garcia A, Parivar K, Hee B, Boni J. Population pharmacokinetics of inotuzumab ozogamicin in relapsed/refractory acute lymphoblastic leukemia and non-Hodgkin lymphoma. J Pharmacokinet Pharmacodyn. 2019;46:211–22.
DeAngelo DJ, Stock W, Stein AS, Shustov A, Liedtke M, Schiffer CA, et al. Inotuzumab ozogamicin in adults with relapsed or refractory CD22-positive acute lymphoblastic leukemia: a phase 1/2 study. Blood Adv. 2017;1:1167–80.
Campana D. Minimal residual disease in acute lymphoblastic leukemia. Semin Hematol. 2009;46:100–6.
Cherian S, Miller V, McCullouch V, Dougherty K, Fromm JR, Wood BL. A novel flow cytometric assay for detection of residual disease in patients with B-lymphoblastic leukemia/lymphoma post anti-CD19 therapy. Cytometry B Clin Cytom. 2018;94:112–20.
Cherian S, Stetler-Stevenson M. Flow cytometric monitoring for residual disease in B lymphoblastic leukemia post T cell engaging targeted therapies. Curr Protoc Cytom. 2018;86:e44.
Jabbour E, Ravandi F, Kebriaei P, Huang X, Short NJ, Thomas D, et al. Salvage chemoimmunotherapy with inotuzumab ozogamicin combined with mini-hyper-CVD for patients with relapsed or refractory Philadelphia chromosome-negative acute lymphoblastic leukemia: a phase 2 clinical trial. JAMA Oncol. 2018;4:230–4.
Jabbour E, Sasaki K, Ravandi F, Huang X, Short NJ, Khouri M, et al. Chemoimmunotherapy with inotuzumab ozogamicin combined with mini-hyper-CVD, with or without blinatumomab, is highly effective in patients with Philadelphia chromosome-negative acute lymphoblastic leukemia in first salvage. Cancer. 2018;124:4044–55.
Kantarjian H, Ravandi F, Short NJ, Huang X, Jain N, Sasaki K, et al. Inotuzumab ozogamicin in combination with low-intensity chemotherapy for older patients with Philadelphia chromosome-negative acute lymphoblastic leukaemia: a single-arm, phase 2 study. Lancet Oncol. 2018;19:240–8.
Kantarjian HM, DeAngelo DJ, Advani AS, Stelljes M, Kebriaei P, Cassaday RD, et al. Hepatic adverse event profile of inotuzumab ozogamicin in adult patients with relapsed or refractory acute lymphoblastic leukaemia: results from the open-label, randomised, phase 3 INO-VATE study. Lancet Haematol. 2017;4:e387–98.
Piccaluga PP, Arpinati M, Candoni A, Laterza C, Paolini S, Gazzola A, et al. Surface antigens analysis reveals significant expression of candidate targets for immunotherapy in adult acute lymphoid leukemia. Leuk Lymphoma. 2011;52:325–7.
Advani A, Coiffier B, Czuczman MS, Dreyling M, Foran J, Gine E, et al. Safety, pharmacokinetics, and preliminary clinical activity of inotuzumab ozogamicin, a novel immunoconjugate for the treatment of B-cell non-Hodgkin's lymphoma: results of a phase I study. J Clin Oncol. 2010;28:2085–93.
Kantarjian H, Thomas D, Jorgensen J, Kebriaei P, Jabbour E, Rytting M, et al. Results of inotuzumab ozogamicin, a CD22 monoclonal antibody, in refractory and relapsed acute lymphocytic leukemia. Cancer. 2013;119:2728–36.
McDonald GB, Freston JW, Boyer JL, DeLeve LD. Liver complications following treatment of hematologic malignancy with anti-CD22-calicheamicin (inotuzumab ozogamicin). Hepatology. 2019;69:831–44.
Kantarjian HM, Thomas D, Ravandi F, Faderl S, Jabbour E, Garcia-Manero G, et al. Defining the course and prognosis of adults with acute lymphocytic leukemia in first salvage after induction failure or short first remission duration. Cancer. 2010;116:5568–74.