Minimal residual disease assessed by multi-parameter flow cytometry is highly prognostic in adult patients with acute lymphoblastic leukaemia

British Journal of Haematology

Volumn 172, Issue 3, 2016, Pages 392-400

  Ravandi, Farhad ^a   Jorgensen, Jeffrey L ^a   O'Brien, Susan M ^a   Jabbour, Elias ^a   Thomas, Deborah A ^a   Borthakur, Gautam ^a   Garris, Rebecca ^a   Huang, Xuelin ^a   Garcia Manero, Guillermo ^a   Burger, Jan A ^a   Ferrajoli, Alessandra ^a   Wierda, William ^a   Kadia, Tapan ^a   Jain, Nitin ^a   Wang, Sa A ^a   Konoplev, Sergei ^a   Kebriaei, Partow ^a   Champlin, Richard E ^a   Mccue, Deborah ^a   Estrov, Zeev ^a   Cortes, Jorge E ^a   Kantarjian, Hagop M ^a   more..

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

Author keywords

Acute leukaemia; Flow cytometry; Minimal residual disease

Indexed keywords

CARCINOEMBRYONIC ANTIGEN RELATED CELL ADHESION MOLECULE 6; CD15 ANTIGEN; CD20 ANTIGEN; CD22 ANTIGEN; CD33 ANTIGEN; CD38 ANTIGEN; CD45 ANTIGEN; CD81 ANTIGEN; COMMON ACUTE LYMPHOBLASTIC LEUKEMIA ANTIGEN; INTERLEUKIN 2 RECEPTOR ALPHA; LYMPHOCYTE FUNCTION ASSOCIATED ANTIGEN 3; MICROSOMAL AMINOPEPTIDASE; ANTINEOPLASTIC AGENT;

ACUTE LYMPHOBLASTIC LEUKEMIA; ADOLESCENT; ADULT; AGE DISTRIBUTION; AGED; ANTIGEN EXPRESSION; ARTICLE; CANCER PROGNOSIS; CANCER REGRESSION; CONTROLLED STUDY; CYTOGENETICS; DIAGNOSTIC TEST ACCURACY STUDY; DISEASE FREE SURVIVAL; FEMALE; FLOW CYTOMETRY; HUMAN; LEUKOCYTE COUNT; MAJOR CLINICAL STUDY; MALE; MINIMAL RESIDUAL DISEASE; OVERALL SURVIVAL; PRIORITY JOURNAL; SENSITIVITY AND SPECIFICITY; MIDDLE AGED; PATHOLOGY; PRECURSOR CELL LYMPHOBLASTIC LEUKEMIA-LYMPHOMA; PROCEDURES; PROGNOSIS; PROSPECTIVE STUDY; REMISSION; TREATMENT OUTCOME; VERY ELDERLY; YOUNG ADULT;

ADOLESCENT; ADULT; AGED; AGED, 80 AND OVER; ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; FEMALE; FLOW CYTOMETRY; HUMANS; LEUKOCYTE COUNT; MALE; MIDDLE AGED; NEOPLASM, RESIDUAL; PRECURSOR CELL LYMPHOBLASTIC LEUKEMIA-LYMPHOMA; PROGNOSIS; PROSPECTIVE STUDIES; REMISSION INDUCTION; TREATMENT OUTCOME; YOUNG ADULT;

EID: 84955727108     PISSN: 00071048     EISSN: 13652141     Source Type: Journal    
DOI: 10.1111/bjh.13834     Document Type: Article

References (36)

1. Armstrong, S.A. & Look, A.T. (2005) Molecular genetics of acute lymphoblastic leukemia. Journal of Clinical Oncology, 23, 6306-6315.
2. Bar, M., Wood, B.L., Radich, J.P., Doney, K.C., Woolfrey, A.E., Delaney, C., Appelbaum, F.R. & Gooley, T.A. (2014) Impact of minimal residual disease, detected by flow cytometry, on outcome of myeloablative hematopoietic cell transplantation for acute lymphoblastic leukemia. Leukemia Research and Treatment, 2014, 421723.
3. Bassan, R. & Hoelzer, D. (2011) Modern therapy of acute lymphoblastic leukemia. Journal of Clinical Oncology, 29, 532-543.
4. Bassan, R., Spinelli, O., Oldani, E., Intermesoli, T., Tosi, M., Peruta, B., Rossi, G., Borlenghi, E., Pogliani, E.M., Terruzzi, E., Fabris, P., Cassibba, V., Lambertenghi-Deliliers, G., Cortelezzi, A., Bosi, A., Gianfaldoni, G., Ciceri, F., Bernardi, M., Gallamini, A., Mattei, D., Di Bona, E., Romani, C., Scattolin, A.M., Barbui, T. & Rambaldi, A. (2009) Improved risk classification for risk-specific therapy based on the molecular study of minimal residual disease (MRD) in adult acute lymphoblastic leukemia (ALL). Blood, 113, 4153-4162.
5. Beldjord, K., Chevret, S., Asnafi, V., Huguet, F., Boulland, M.L., Leguay, T., Thomas, X., Cayuela, J.M., Grardel, N., Chalandon, Y., Boissel, N., Schaefer, B., Delabesse, E., Cavé, H., Chevallier, P., Buzyn, A., Fest, T., Reman, O., Vernant, J.P., Lhéritier, V., Béné, M.C., Lafage, M., Macintyre, E., Ifrah, N. & Dombret, H.; Group for Research on Adult Acute Lymphoblastic Leukemia (GRAALL). (2014) Oncogenetics and minimal residual disease are independent outcome predictors in adult patients with acute lymphoblastic leukemia. Blood, 123, 3739-3749.
6. Bruggemann, M., Raff, T., Flohr, T., Gokbuget, N., Nakao, M., Droese, J., Lüschen, S., Pott, C., Ritgen, M., Scheuring, U., Horst, H.A., Thiel, E., Hoelzer, D., Bartram, C.R. & Kneba, M.; German Multicenter Study Group for Adult Acute Lymphoblastic Leukemia. (2006) Clinical significance of minimal residual disease quantification in adult patients with standard-risk acute lymphoblastic leukemia. Blood, 107, 1116-1123.
7. Bruggemann, M., Raff, T. & Kneba, M. (2012) Has MRD monitoring superseded other prognostic factors in adult ALL? Blood, 120, 4470-4481.
8. Campana, D. (2010) Minimal residual disease in acute lymphoblastic leukemia. Hematology/the Education Program of the American Society of Hematology. American Society of Hematology, 2010, 7-12.
9. Cox, D.R. (1972) Regression models and life-tables. Journal of the Royal Statistical Society Series B (Methodological), 34, 187-220.
10. Curran, E. & Stock, W. (2015) How I Treat: acute lymphoblastic leukemia in older Adolescents and Young Adults (AYAs). Blood, 125, 3702-3710.
11. Dafni, U. (2011) Primer on statistical interpretation and methods: landmark analysis at the 25-year landmark point. Circulation: Cardiovascular Quality and Outcomes, 4, 363-371.
12. Fielding, A.K., Richards, S.M., Chopra, R., Lazarus, H.M., Litzow, M.R., Buck, G., Durrant, I.J., Luger, S.M., Marks, D.I., Franklin, I.M., McMillan, A.K., Tallman, M.S., Rowe, J.M. & Goldstone, A.H.; Medical Research Council of the United Kingdom Adult ALL Working Party; Eastern Cooperative Oncology Group. (2007) Outcome of 609 adults after relapse of acute lymphoblastic leukemia (ALL); an MRC UKALL12/ECOG 2993 study. Blood, 109, 944-950.
13. Gajjar, A., Ribeiro, R., Hancock, M.L., Rivera, G.K., Mahmoud, H., Sandlund, J.T., Crist, W.M. & Pui, C.H. (1995) Persistence of circulating blasts after 1 week of multiagent chemotherapy confers a poor prognosis in childhood acute lymphoblastic leukemia. Blood, 86, 1292-1295.
14. Gokbuget, N., Stanze, D., Beck, J., Diedrich, H., Horst, H.A., Huttmann, A., Kobbe, G., Kreuzer, K.A., Leimer, L., Reichle, A., Schaich, M., Schwartz, S., Serve, H., Starck, M., Stelljes, M., Stuhlmann, R., Viardot, A., Wendelin, K., Freund, M. & Hoelzer, D.; German Multicenter Study Group for Adult Acute Lymphoblastic Leukemia. (2012a) Outcome of relapsed adult lymphoblastic leukemia depends on response to salvage chemotherapy, prognostic factors, and performance of stem cell transplantation. Blood, 120, 2032-2041.
15. Gokbuget, N., Kneba, M., Raff, T., Trautmann, H., Bartram, C.R., Arnold, R., Fietkau, R., Freund, M., Ganser, A., Ludwig, W.D., Maschmeyer, G., Rieder, H., Schwartz, S., Serve, H., Thiel, E., Brüggemann, M. & Hoelzer, D.; German Multicenter Study Group for Adult Acute Lymphoblastic Leukemia. (2012b) Adult patients with acute lymphoblastic leukemia and molecular failure display a poor prognosis and are candidates for stem cell transplantation and targeted therapies. Blood, 120, 1868-1876.
16. Grupp, S.A., Kalos, M., Barrett, D., Aplenc, R., Porter, D.L., Rheingold, S.R., Teachey, D.T., Chew, A., Hauck, B., Wright, J.F., Milone, M.C., Levine, B.L. & June, C.H. (2013) Chimeric antigen receptor-modified T cells for acute lymphoid leukemia. New England Journal of Medicine, 368, 1509-1518.
17. Kantarjian, H.M., O'Brien, S., Smith, T.L., Cortes, J., Giles, F.J., Beran, M., Pierce, S., Huh, Y., Andreeff, M., Koller, C., Ha, C.S., Keating, M.J., Murphy, S. & Freireich, E.J. (2000) Results of treatment with hyper-CVAD, a dose-intensive regimen, in adult acute lymphocytic leukemia. Journal of Clinical Oncology, 18, 547-561.
18. Kantarjian, H., Thomas, D., Wayne, A.S. & O'Brien, S. (2012) Monoclonal antibody-based therapies: a new dawn in the treatment of acute lymphoblastic leukemia. Journal of Clinical Oncology, 30, 3876-3883.
19. Moorman, A.V., Enshaei, A., Schwab, C., Wade, R., Chilton, L., Elliott, A., Richardson, S., Hancock, J., Kinsey, S.E., Mitchell, C.D., Goulden, N., Vora, A. & Harrison, C.J. (2014) A novel integrated cytogenetic and genomic classification refines risk stratification in pediatric acute lymphoblastic leukemia. Blood, 124, 1434-1444.
20. Nachman, J.B., Sather, H.N., Sensel, M.G., Trigg, M.E., Cherlow, J.M., Lukens, J.N., Wolff, L., Uckun, F.M. & Gaynon, P.S. (1998) Augmented post-induction therapy for children with high-risk acute lymphoblastic leukemia and a slow response to initial therapy. New England Journal of Medicine, 338, 1663-1671.
21. O'Brien, S., Thomas, D., Ravandi, F., Faderl, S., Cortes, J., Borthakur, G., Pierce, S., Garcia-Manero, G. & Kantarjian, H.M. (2008a) Outcome of adults with acute lymphocytic leukemia after second salvage therapy. Cancer, 113, 3186-3191.
22. O'Brien, S., Thomas, D.A., Ravandi, F., Faderl, S., Pierce, S. & Kantarjian, H. (2008b) Results of the hyperfractionated cyclophosphamide, vincristine, doxorubicin, and dexamethasone regimen in elderly patients with acute lymphocytic leukemia. Cancer, 113, 2097-2101.
23. Paganin, M., Fabbri, G., Conter, V., Barisone, E., Polato, K., Cazzaniga, G., Giraldi, E., Fagioli, F., Aricò, M., Valsecchi, M.G. & Basso, G. (2014) Postinduction minimal residual disease monitoring by polymerase chain reaction in children with acute lymphoblastic leukemia. Journal of Clinical Oncology, 32, 3553-3558.
24. Patel, B., Rai, L., Buck, G., Richards, S.M., Mortuza, Y., Mitchell, W., Gerrard, G., Moorman, A.V., Duke, V., Hoffbrand, A.V., Fielding, A.K., Goldstone, A.H. & Foroni, L. (2010) Minimal residual disease is a significant predictor of treatment failure in non T-lineage adult acute lymphoblastic leukaemia: final results of the international trial UKALL XII/ECOG2993. British Journal of Haematology, 148, 80-89.
25. Pui, C.H. & Evans, W.E. (2006) Treatment of acute lymphoblastic leukemia. New England Journal of Medicine, 354, 166-178.
26. Pui, C.H., Pei, D., Coustan-Smith, E., Jeha, S., Cheng, C., Bowman, W.P., Sandlund, J.T., Ribeiro, R.C., Rubnitz, J.E., Inaba, H., Bhojwani, D., Gruber, T.A., Leung, W.H., Downing, J.R., Evans, W.E., Relling, M.V. & Campana, D. (2015) Clinical utility of sequential minimal residual disease measurements in the context of risk-based therapy in childhood acute lymphoblastic leukaemia: a prospective study. The Lancet. Oncology, 16, 465-474.
27. Ribera, J.M., Oriol, A., Morgades, M., Montesinos, P., Sarra, J., Gonzalez-Campos, J., Brunet, S., Tormo, M., Fernández-Abellán, P., Guàrdia, R., Bernal, M.T., Esteve, J., Barba, P., Moreno, M.J., Bermúdez, A., Cladera, A., Escoda, L., García-Boyero, R., Del Potro, E., Bergua, J., Amigo, M.L., Grande, C., Rabuñal, M.J., Hernández-Rivas, J.M. & Feliu, E. (2014) Treatment of high-risk Philadelphia chromosome-negative acute lymphoblastic leukemia in adolescents and adults according to early cytologic response and minimal residual disease after consolidation assessed by flow cytometry: final results of the PETHEMA ALL-AR-03 trial. Journal of Clinical Oncology, 32, 1595-1604.
28. Roberts, K.G., Li, Y., Payne-Turner, D., Harvey, R.C., Yang, Y.L., Pei, D., McCastlain, K., Ding, L., Lu, C., Song, G., Ma, J., Becksfort, J., Rusch, M., Chen, S.C., Easton, J., Cheng, J., Boggs, K., Santiago-Morales, N., Iacobucci, I., Fulton, R.S., Wen, J., Valentine, M., Cheng, C., Paugh, S.W., Devidas, M., Chen, I.M., Reshmi, S., Smith, A., Hedlund, E., Gupta, P., Nagahawatte, P., Wu, G., Chen, X., Yergeau, D., Vadodaria, B., Mulder, H., Winick, N.J., Larsen, E.C., Carroll, W.L., Heerema, N.A., Carroll, A.J., Grayson, G., Tasian, S.K., Moore, A.S., Keller, F., Frei-Jones, M., Whitlock, J.A., Raetz, E.A., White, D.L., Hughes, T.P., Guidry Auvil, J.M., Smith, M.A., Marcucci, G., Bloomfield, C.D., Mrózek, K., Kohlschmidt, J., Stock, W., Kornblau, S.M., Konopleva, M., Paietta, E., Pui, C.H., Jeha, S., Relling, M.V., Evans, W.E., Gerhard, D.S., Gastier-Foster, J.M., Mardis, E., Wilson, R.K., Loh, M.L., Downing, J.R., Hunger, S.P., Willman, C.L., Zhang, J. & Mullighan, C.G. (2014a) Targetable kinase-activating lesions in Ph-like acute lymphoblastic leukemia. New England Journal of Medicine, 371, 1005-1015.
29. Roberts, K.G., Pei, D., Campana, D., Payne-Turner, D., Li, Y., Cheng, C., Sandlund, J.T., Jeha, S., Easton, J., Becksfort, J., Zhang, J., Coustan-Smith, E., Raimondi, S.C., Leung, W.H., Relling, M.V., Evans, W.E., Downing, J.R., Mullighan, C.G. & Pui, C.H. (2014b) Outcomes of children with BCR-ABL1-like acute lymphoblastic leukemia treated with risk-directed therapy based on the levels of minimal residual disease. Journal of Clinical Oncology, 32, 3012-3020.
30. Schrappe, M. (2014) Detection and management of minimal residual disease in acute lymphoblastic leukemia. Hematology/the Education Program of the American Society of Hematology. American Society of Hematology, 2014, 244-249.
31. Stow, P., Key, L., Chen, X., Pan, Q., Neale, G.A., Coustan-Smith, E., Mullighan, C.G., Zhou, Y., Pui, C.H. & Campana, D. (2010) Clinical significance of low levels of minimal residual disease at the end of remission induction therapy in childhood acute lymphoblastic leukemia. Blood, 115, 4657-4663.
32. Topp, M.S., Kufer, P., Gokbuget, N., Goebeler, M., Klinger, M., Neumann, S., Horst, H.A., Raff, T., Viardot, A., Schmid, M., Stelljes, M., Schaich, M., Degenhard, E., Köhne-Volland, R., Brüggemann, M., Ottmann, O., Pfeifer, H., Burmeister, T., Nagorsen, D., Schmidt, M., Lutterbuese, R., Reinhardt, C., Baeuerle, P.A., Kneba, M., Einsele, H., Riethmüller, G., Hoelzer, D., Zugmaier, G. & Bargou, R.C. (2011) Targeted therapy with the T-cell-engaging antibody blinatumomab of chemotherapy-refractory minimal residual disease in B-lineage acute lymphoblastic leukemia patients results in high response rate and prolonged leukemia-free survival. Journal of Clinical Oncology, 29, 2493-2498.
33. Vora, A., Goulden, N., Mitchell, C., Hancock, J., Hough, R., Rowntree, C., Moorman, A.V. & Wade, R. (2014) Augmented post-remission therapy for a minimal residual disease-defined high-risk subgroup of children and young people with clinical standard-risk and intermediate-risk acute lymphoblastic leukaemia (UKALL 2003): a randomised controlled trial. The Lancet. Oncology, 15, 809-818.
34. Weir, E.G., Cowan, K., LeBeau, P. & Borowitz, M.J. (1999) A limited antibody panel can distinguish B-precursor acute lymphoblastic leukemia from normal B precursors with four color flow cytometry: implications for residual disease detection. Leukemia, 13, 558-567.
35. Yeoh, A.E., Ariffin, H., Chai, E.L., Kwok, C.S., Chan, Y.H., Ponnudurai, K., Campana, D., Tan, P.L., Chan, M.Y., Kham, S.K., Chong, L.A., Tan, A.M., Lin, H.P. & Quah, T.C. (2012) Minimal residual disease-guided treatment deintensification for children with acute lymphoblastic leukemia: results from the Malaysia-Singapore acute lymphoblastic leukemia 2003 study. Journal of Clinical Oncology, 30, 2384-2392.
36. Zhou, Y., Slack, R., Jorgensen, J.L., Wang, S.A., Rondon, G., de Lima, M., Shpall, E., Popat, U., Ciurea, S., Alousi, A., Qazilbash, M., Hosing, C., O'Brien, S., Thomas, D., Kantarjian, H., Medeiros, L.J., Champlin, R.E. & Kebriaei, P. (2014) The effect of peritransplant minimal residual disease in adults with acute lymphoblastic leukemia undergoing allogeneic hematopoietic stem cell transplantation. Clinical Lymphoma, Myeloma and Leukemia, 14, 319-326.