Minimal residual disease status as a predictor of relapse after allogeneic bone marrow transplantation for children with acute lymphoblastic leukaemia

British Journal of Haematology

Volumn 102, Issue 3, 1998, Pages 860-871

  Knechtli, Christopher J C ^a,b   Goulden, Nicholas J ^a,b   Hancock, Jeremy P ^a   Harris, Emma L ^a   Garland, Russell J ^a   Jones, Claire G ^a   Grandage, Victoria L G ^a,b   Rowbottom, Anthony W ^a   Green, Ann F ^c   Clarke, Emer ^c   Lankester, Alan W ^c   Potter, Michael N ^b   Cornish, Jacqueline M ^b   Pamphilon, Derwood H ^b,c   Steward, Colin G ^a,b   Oakhill, Anthony ^b  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

^b BRISTOL ROYAL HOSPITAL FOR CHILDREN   (United Kingdom)

^c NHS BLOOD AND TRANSPLANT   (United Kingdom)

Author keywords

Acute lymphoblastic leukaemia; Allogeneic bone marrow transplant; Minimal residual disease; Polymerase chain reaction

Indexed keywords

ACUTE LYMPHOBLASTIC LEUKEMIA; ALLOGENIC BONE MARROW TRANSPLANTATION; ARTICLE; BONE MARROW TRANSPLANTATION; CANCER RECURRENCE; CHILD; CONTROLLED STUDY; DISEASE ACTIVITY; HUMAN; MAJOR CLINICAL STUDY; MORTALITY; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROGNOSIS;

ADOLESCENT; BONE MARROW TRANSPLANTATION; CHILD; CHILD, PRESCHOOL; HUMANS; INFANT; INFANT, NEWBORN; LEUKEMIA, LYMPHOCYTIC, ACUTE, L1; NEOPLASM, RESIDUAL; OLIGONUCLEOTIDE PROBES; POLYMERASE CHAIN REACTION; RECURRENCE; TRANSPLANTATION, HOMOLOGOUS;

EID: 7344259636     PISSN: 00071048     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-2141.1998.00873.x     Document Type: Article

References (70)

1. Atra, A., Millar, B., Shepherd, V., Shankar, A., Wilson, K., Treleaven, J., Pritchard-Jones, K., Meller, S.T. & Pinkerton, C.R. (1997) Donor lymphocyte infusion for childhood acute lymphoblastic leukaemia relapsing after bone marrow transplantation. British Journal of Haematology, 97, 165-168.
2. Balduzzi, A., Gooley, T., Anasetti, C., Sanders, J.E., Martin, P.J., Petersdorf, E.W., Appelbaum, F.R., Buckner, C.D., Mathews, D. & Storb, R. (1995) Unrelated donor marrow transplantation in children. Blood, 86, 3247-3256.
3. Barrett, A.J. (1994) Bone marrow transplantation from acute lymphoblastic leukaemia. Bailliere's Clinical Haematology, 7, 377-401.
4. Barrett, A.J., Horowitz, M.M., Pollock, B.H., Zhang, M.J., Bortin, M.M., Buchanan, G.R., Camitta, B.M., Ochs, J., Graham-Pole, J. & Rowlings, P.A. (1994) Bone marrow transplants from HLA-identical siblings as compared with chemotherapy for children with acute lymphoblastic leukemia in a second remission. New England Journal of Medicine, 331, 1253-1258.
5. Barrett, A.J. & Malkovska, V. (1996) Graft-versus-leukaemia: understanding and using the alloimmune response to treat haematological malignancies. British Journal of Haematology, 93, 754-761.
6. Barrett, A.J. & van Rhee, E. (1997) Graft-versus-leukaemia. Balliere's Clinical Haematology, 10, 337-355.
7. Bartram, C.R. (1993) Detection of minimal residual leukemia by the polymerase chain reaction: potential implications for therapy. Clinica Chimica Acta, 217, 75-83.
8. Beishuizen, A., Verhoeven, M.A., Hahlen, K., van Wering, E.R. & van Dongen, J.J. (1993) Differences in immunoglohulin heavy chain gene rearrangment patterns between bone marrow and blood samples in childhood precursor B-acute lymphoblastic leukemia at diagnosis. Leukemia, 7, 60-63.
9. Bennett, J.M., Catovsky, D., Daniel, M.T., Flandrin, G., Galton, D.A., Gralnick, H.R. & Sultan, C. (1976) Proposals for the classification of the acute leukaemias. French-American-British (FAB) co-operative group. British Journal of Haematology, 33, 451-458.
10. Brisco, M.J., Condon, J., Hughes, E., Neoh, S.H., Sykes, H.J., Seshadri, R., Toogood, I., Waters, K., Tauro, G., Ekert, H. & Morley, A.A. (1994) Outcome prediction in childhood acute lymphoblastic leukaemia by molecular quantification of residual disease at the end of induction. Lancet, 343, 196-200.
11. Campana, D., Coustan-Smith, E. & Janossy, G. (1990) Immunophenotyping in haematological diagnosis. Bailliere's Clinical Haematology, 3, 889-919.
12. Campana, D. & Pui, C.H. (1995) Detection of minimal residual disease in acute leukemia: methodological advances and clinical significance. Blood, 85, 1416-1434.
13. Cavé, H., Guidal, C., Rohrlich, P., Delfau, M.H., Broyart, A., Lescoeur, B., Rahimy, C., Fenneteau, O., Monplaisir, N., d'Auriol, L., Elion, J., Vilmer, E. & Grandchamp, B. (1994) Prospective monitoring and quantitation of residual blasts in childhood acute lymphoblastic leukemia by polymerase chain reaction study of delta and gamma T-cell receptor genes. Blood, 83, 1892-1902.
14. Chao, N.J., Forman, S.J., Schmidt, G.M., Snyder, D.S., Amylon, M.D., Konrad, P.N., Nademanee, A.P., O'Donnell, M.R., Parker, P.M. & Stein, A.S. (1991) Allogeneic bone marrow transplantation for high-risk acute lymphoblastic leukemia during first complete remission. Blood, 78, 1923-1927.
15. Chessells, J.M., Richards, S.M., Bailey, C.C., Lilleyman, J.S. & Eden, O.B. (1995) Gender and treatment outcome in childhood lymphoblastic leukaemia: report from the MRC UKALL trials. British Journal of Haematology, 89, 364-372.
16. Choi, Y., Greenberg, S.J., Du, T.L., Ward, P.M., Overturf, P.M., Brecher, M.L. & Ballow, M. (1996) Clonal evolution in B-lineage acute lymphoblastic leukemia by contemporaneous VH-VH gene replacements and VH-DJH gene arrangements. Blood, 87, 2506-2512.
17. Cole-Sinclair, M.F., Foroni, L. & Hoffbrand, A.V. (1994) Genetic-changes: relevance for diagnosis and detection of minimal residual disease in acute lymphoblastic leukaemia. Bailliere's Clinical Haematology, 7, 183-233.
18. Collins, R.H.J., Shpilberg, O., Drobyski, W.R., Porter, D.L., Giralt, S., Champlin, R., Goodman, S.A., Wolff, S.N., Hu, W., Verfaillie, C., List, A., Dalton, Ognoskie, N., Chetrit, A., Antin, J.H. & Nemunaitis, J. (1997) Donor leukocyte infusions in 140 patients with relapsed malignancy after allogeneic bone marrow transplantation. Journal of Clincial Oncology, 15, 433-444.
19. Cross, N.C. (1997) Assessing residual leukaemia. Bailliere's Clinical Haematology, 10, 389-403.
20. d'Hondt, L., Chatelain, C., Doyen, C., Osselaer, J.C., Ferrant, A. & Bosly, A. (1996) Transient complete remission of acute lymphoblastic leukemia in relapse after allogeneic bone marrow transplantation induced by donor leukocyte transfusions. Hematology and Cell Therapy, 38, 353-354.
21. Evans, P.A.S., Forsyth, P.D., Short, M.A., Owen, R.G., Shiach, C.R., Kinsey, S., Davies, F.E., Jack, A.S., Hillmen, P. & Morgan, G.J. (1997) Minimal residual disease detection using a fluorescent concensus IgH PCR at week 20 of therapy is strongly predictive of relapse in children with precursor B-ALL. (Abstract). Blood, 90, (Suppl. 1), 422a.
22. Faber, L.M., van Luxemburg-Heijs, S.A., Willemze, R. & Falkenburg, J.H. (1992) Generation of leukemia-reactivity cytotoxic T lymphocyte clones from the HLA-identical bone marrow donor of a patient with leukemia. Journal of Experimental Medicine, 176, 1283-1284.
23. Ferster, A., Bujan, W. Mouraux, T., Devalck, C., Heimann, P. & Sariban, E. (1994) Complete remission following donor leukocyte infusion in ALL relapsing after haploidentical bone marrow transplantation. Bone Marrow Transplantation, 14, 331-332.
24. Foa, R., Fierro, M.T., Cesano, A., Guarini, A., Bonferroni, M., Raspadori, D., Miniero, R., Lauria, F. & Gavosto, F. (1991) Defective lymphokine-activated killer cell generation and activity in acute leukemia patients with active disease. Blood, 78, 1041-1046.
25. Foot, A.B., Potter, M.N., Donaldson, C., Cornish, J.M., Wallington, T.B., Oakhill, A. & Pamphilon, D.H. (1993) Immune reconstitution after BMT in children. Bone Marrow Transplantation, 11, 7-13.
26. Ghali, D.W., Panzer, S., Fischer, S., Argyriou-Tirita, A., Haas, O.A., Kovar, H., Gadner, H. & Panzer-Grumayer, E.R. (1995) Heterogeneity of the T-cell receptor delta gene indicating subclone formation in acute precursor B-cell leukemias. Blood, 85, 2795-2801.
27. Giralt, S., Hester, J., Huh, Y., Hirsch-Ginsberg, C., Rondon, G., Seong, D., Lee, Gajewski, J., van, B.K. & Khouri, I. (1995) CD8-depleted donor lymphocyte infusion as treatment for relapsed chronic myelogenous leukemia after allogeneic bone marrow transplantation. Blood, 86, 4337-4343.
28. Giralt, S.A. & Kolb, H.J. (1996) Donor lymphocyte infusions. Current Opinion in Oncology, 8, 96-102.
29. Glucksberg, H., Storb, R., Fefer, A., Buckner, C.D., Neiman, P.E., Clift, B.A., Lerner, K.G. & Thomas, E.D. (1974) Clinical manifestations of graft-versus-host disease in human recipients of marrow from HL-A-matched sibling donors. Transplantation, 18, 295-304.
30. Goulden, N., Langlands, K., Steward, C., Katz, F., Potter, M., Chessels, J. & Oakhill, A. (1994) PCR assessment of bone marrow status in 'isolated' extramedullarly relapse of childhood B-precursor acute lymphoblastic leukaemia. British Journal of Haematology, 87, 282-285.
31. Goulden, N.J., Knechtli, C.J.C., Garland, R.J., Langlands, K., Hancock, J.P., Potter, M.N., Steward, C.G. & Oakhill, A. (1998) Minimal residual disease analysis for the prediction of relapse in children with standard-risk acute lymphoblastic leukaemia. British Journal of Haematology, 100, 235-244.
32. Guglielmi, C., Cordone, I., Boecklin, F., Masi, S., Valentini, T., Vegna, M.U., Ferrari, A., Testi, A.M. & Foa, R. (1997) Immunophenotype of adult and childhood acute lymphoblastic leukemia: changes at first relapse and clinico-prognostic implications. Leukemia, 11, 1501-1507.
33. Horowitz, M.M., Gale, R.P., Sondel, P.M., Goldman, J.M., Kersey, J., Kolb, H.J., Rimm, A.A., Ringden, O., Rozman, C. & Speck, B. (1990) Graft-versus-leukemia reactions after bone marrow transplantation. Blood, 75, 555-562.
34. Jorgensen, H., Hokland, P. Jensen, A.W. & Hokland, M. (1996) Little evidence for clonal evolution of malignant haematopoietic cells following relapse after autologous bone marrow transplantation. European Journal of Haematology, 57, 25-32.
35. Keil, F., Kalhs, P., Haas, O.A., Fritsch, G., Reiter, E., Mannhalter, C., Lechner, Leitner, G. & Greinix, H.T. (1997) Relapse of Philadelphia chromosome positive acute lymphoblastic leukaemia after marrow transplantation: sustained molecular remission after early and dose-escalating infusion of donor leucocytes. British Journal of Haematology, 97, 161-164.
36. Kiyoi, H., Naoe, T., Kitamura, K., Yamauchi, T., Ichihashi, T. & Ohno, R. (1991) Disappearance of minimal residual lymphoblastic leukemia cells 6 months after allogeneic bone marrow transplantation without GVHD. Bone Marrow Transplantation, 8, 59-62.
37. Knechtli, C.J.C., Goulden, N.J., Langlands, K. & Potter, M.N. (1995) The study of minimal residual disease in acute lymphoblastic leukaemia. Journal of Clinical Pathology-Molecular Pathology, 48, M65-M73.
38. Kolb, H.J., Schattenberg, A., Goldman, J.M., Hertenstein, B., Jacobsen, N., Arcese, W., Ljungman, P., Ferrant, A., Verdonck, L. & Niederwieser, D. (1995) Graft-versus-leukemia effect of donor lymphocyte transfusions in marrow grafted patients. European Group for Blood and Marrow Transplantation Working Party Chronic leukemia. Blood, 86, 2041-2050.
39. Mackinnon, S. (1997) Donor leukocyte infusions. Bailliere's Clinical Haematology, 10, 357-567.
40. Mackinnon, S., Papadopoulos, E.B., Carabasi, M.H., Reich, L. Collins, N.H., Boulad, E. Castro-Malaspina, H., Childs, B.H., Gillio, A.P., Kernan, N.A., Small, T.N., Young, J.W. & O'Reilly, R.J. (1995) Adoptive immunotherapy evaluating escalating doses of donor leukocytes for relapse of chronic myeloid leukemia after bone marrow transplantation: separation of graft-versus-leukemia responses from graft-versus-host disease. Blood, 86, 1261-1268.
41. Marshall, G.M., Kwan, E., Haber, M., Brisco, M.J., Sykes, P.J., Morley, A.A., Toogood, I., Waters, K., Tauro, G., Ekert, H. & Norris, M.D. (1995) Characterization of clonal immunoglobulin heavy chain and T cell receptor gamma gene rearrangements during progression of childhood acute lymphoblastic leukemia. Leukemia, 9, 1847-1850.
42. Naparstek, E., Or, R., Magler, A., Cividalli, G., Engelhard, D., Aker, M., Gimon, Z., Manny, N., Sacks, T., Tochner, Z., Weiss, L., Samuel, S.. Brautbar, C.. Hale, G., Waldmann, H., Steinberg, S.M. & Slavin, S. (1995) T-cell-depleted allogeneic bone marrow transplantation for acute leukaemia using Campath-1 antibodies and post-transplant administration of donor's peripheral blood lymphocytes for prevention of relapse. British Journal of Haematology, 89, 506-515.
43. Neale, G.A.M., Pui, C.H., Mahmoud, H.H., Mirro J Jr, Crist, W.M., Rivera, G.K. & Goorha, R.M. (1994) Molecular evidence for minimal residual bone marrow disease in children with 'isolated' extramedullary relapse of T-cell acute lymphoblastic leukemia. Leukemia, 8, 768-775.
44. Nizet, Y., Martiat, P., Vaerman, J.L. Philippe, M., Wildmann, C. Staelens, J.P., Cornu, G., Ferrant, A., Michaux, J.L. & Sokal, G. (1991) Follow-up of residual disease (MRD) in B lineage acute leukaemias using a simplitied PCR strategy: evolution of MRD rather than its detection is correlated with clinical outcome. British Journal of Haematology, 79, 205-210.
45. Nizet, Y., Van Daele, S.,Lewalle, P., Vaerman, J.L., Philippe, M., Vermylen, C., Cornu, G., Ferrant, A., Michaux, J.L. & Martiat, P. (1993) Long-term follow-up of residual disease in acute lymphoblastic leukemia patients in complete remission using clonogeneic IgH probes and the polymerase chain reaction. Blood, 82, 1618-1625.
46. Oakhill, A., Pamphilon, D.H., Potter, M.N., Steward, C.G., Goodman, S., Green, A., Goulden, P. Goulden, N.J., Hale, G., Waldmann, H. & Cornish, J.M. (1996) Unrelated donor bone marrow transplantation for children with relapsed acute lymphoblastic leukaemia in second complete remission. British Journal of Haematology, 94, 574-578.
47. Papaionnou, M., Coyle, L.A., Yaxley, J.C., Prentice, H.G., Mehta, A., Hoffbrand, A.V. & Foroni, L. (1997) Molecular detection of minimal residual disease in adult and childhood acute lymphoblastic leukaemia reveals differences in treatment response. (Abstract). British Journal of Haematology, 97, 45.
48. Plautz, G., Nabel, E.G. & Nabel, G.J. (1991) Selective elimination of recombinant genes in vivo with a suicide retroviral vector. New Biologist, 3, 709-715.
49. Porter, D.L., Roth, M.S., McGarigle, C., Ferrara, J.L. & Antin, J.H. (1994) Induction of graft-versus-host disease as immunotherapy for relapsed chronic myeloid leukemia. New England Journal of Medicine, 330, 100-106.
50. Preudhomme, C., Henic, N., Cazin, B., Lai, J.L., Bertheas, M.F., Vanrumbeke, M., Lemoine, F., Jouet, J.P., Deconninck, E., Nelken, B., Cosson, A. & Fenaux, P. (1997) Good correlation between RT-PCR analysis and relapse in Philadelphia (Ph1)-positive acute lymphoblastic leukemia (ALL). Leukemia, 11, 294-298.
51. Radich, J., Ladne, P. & Gooley, T. (1995) Polymerase chain reaction-based detection of minimal residual disease in acute lymphoblastic leukemia predicts relapse after allogeneic BMT. Biology of Blood and Marrow Transplantation, 1, 24-31.
52. Roberts, W.M., Estrov, Z., Kitchingman, G.R. & Zipf, T.F. (1996) The clinical significance of residual disease in childhood acute lymphoblastic leukemia as detected by polymerase chain reaction amplification by antigen-receptor gene sequences. Leukemia and Lymphoma, 20, 181-197.
53. Roberts, W.M., Estrov, Z., Ouspenskaia, M.V., Johnston, D.A., McClain, K.L. & Zipf, T.F. (1997) Measurement of residual leukemia during remission in childhood acute lymphoblastic leukemia. New England Journal of Medicine, 336, 317-323.
54. Rooney, C.M., Smith, C.A., Ng, C.Y., Loftin, S., Li, C., Krance, R.A., Brenner, M.K. & Heslop, H.E. (1995) Use of gene-modified virus-specific T lymphocytes to control Epstein-Barr-virus-related lymphoproliferation. Lancet, 345, 9-13.
55. Sambrook, J., Fritsch, E.F. & Maniatis, T. (1989) Commonly used techniques in molecular cloning. Molecular Cloning: a Laboratory Manual (ed. by J. Sambrook, E. F. Fritsch and T. Maniatis), p. E3. Cold Spring Harbour Laboratory Press, New York.
56. Secker-Walker, L.M., Lawler, S.D. & Hardisty, R.M. (1978) Prognostic implications of chromosomal findings in acute lymphoblastic leukaemia at diagnosis. British Medical Journal, ii, 1529-1530.
57. Seriu, T., Yokota, S., Nakao, M., Misawa, S., Takaue, Y., Koizumi, S., Kawai, S. & Fujimoto, T. (1995) Prospective monitoring of minimal residual disease during the course of chemotherapy in patients with acute lymphoblastic leukemia, and detection of contaminating tumor cells in peripheral blood stem cells for autotransplantation. Leukemia, 9, 615-623.
58. Shulman, H.M., Sullivan, K.M., Weiden, P.L., McDonald, E.B., Striker, G.E., Sale, G.E., Hachman, R., Tosoi, M., Storb, R. & Thomas, E.D. (1980) Chronic graft versus host syndrome in man: a long-term clinicopathological study in 20 Seattle patients. American Journal of Medicine, 69, 204-217.
59. Slavin, S., Naparstek, E., Nagler, A., Ackerstein, A., Kapelushnik, J. & Or, R. (1995) Allogencic cell therapy for relapsed leukemia after bone marrow transplantation with donor peripheral blood lymphocytes. Experimental Hematology, 23, 1553-1562.
60. Slavin, S., Naparstek, E., Nagler, A., Ackerstein, A., Samuel, S., Kapelushnik, J., Brautbar, C. & Or, R. (1996) Allogeneic cell therapy with donor peripheral blood cells and recombinant human interleukin-2 to treat leukemia relapse after allogeneic bone marrow transplantation. Blood, 87, 2195-2204.
61. Sosman, J.A., Oettel, K.R., Smith, S.D., Hank, J.A., Fisch, P. & Sondel, P.M. (1990) Specific recognition of human leukemic cells by allogeneic T cells. II. Evidence for HLA-D restricted determinants on leukemic cells that are crossreactive with determinants present on unrelated nonleukemic cells. Blood. 75, 2005-2016.
62. Steenbergen, E.J., Verhagen, O.J., van Leeuwen, E.F., van den Berg, H., Behrendt, H., Slater, R.M., von dem Borne, A.E. & van der Schoot, C.E. (1995) Prolonged persistence of PCR-detectable minimal residual disease after diagnosis or first relapse predicts poor outcome in childhood B-precursor acute lymphoblastic leukemia. Leukemia, 9, 1726-1734.
63. Steenbergen, E.J., Verhagen, O.J., van Leeuwen, E.F., von dem Borne, A.E. & van der School, C.E. (1993) Distinct ongoing Ig heavy chain rearrangement processes in childhood B-precursor acute lymphoblastic leukemia. Blood, 82, 581-589.
64. Steward, C.G., Goulden, N.J., Katz, P., Baines, D., Martin, P.G., Langlands, K., Potter, M.N., Chessells, J.M. & Oakhill, A. (1994) A polymerase chain reaction study of the stability of Ig heavy-chain and T-cell receptor delta gene rearrangements between presentation and relapse of childhood B-lineage acute lymphoblastic leukemia. Blood, 83, 1355-1362.
65. Taylor, J.J., Rowe, D., Kylefjord, H., Chessells, J., Katz, F., Proctor, S.J. & Middleton, P.G. (1994) Characterisation of non-concordance in the T-cell receptor gamma chain genes at presentation and clinical relapse in acute lymphoblastic leukemia. Leukemia, 8, 60-66.
66. Tiberghien, P., Reynolds, C.W., Keller, J., Spence, S., Deschaseaux, M., Certoux, J.M., Contassot, E., Murphy, W.J., Lyons, R. & Chiang, Y. (1994) Ganciclovir treatment of herpes simplex thymidine kinase-transduced primary T lymphocytes: an approach for specific in vivo donor T-cell depletion after bone marrow transplantation? Blood, 84, 1333-1341.
67. Tzeng, C.H., Lin, J.S., Lee, J.C., Yung, C.H., Hu, H.Y. & Chen, P.M. (1996) Transfusion of donor peripheral blood buffy coat cells as effective treatment for relapsed acute leukemia after transplantation of allogeneic bone marrow or peripheral blood stem cells from the same donor. Transfusion, 36, 685-690.
68. van Rhee, F., Lin, F., Cullis, J.O., Spencer, A., Cross, N.C., Chase, A., Garicochea, B., Bungey, J., Barrett, J. & Goldman, J.M. (1994) Relapse of chronic myeloid leukemia after allogeneic bone marrow transplant: the case for giving donor leukocyte transfusions before the onset of hematologic relapse. Blood, 85, 3377-3383.
69. van Wering, E.R., Beishuizen, A., Roeffen, E.T., van der Linden-Schrever, B.E., Verhoeven, M.A., Hahlen, K., Hooijkaas, H. & van Dongen, J.J. (1995) Immunophenotypic changes between diagnosis and relapse in childhood acute lymphoblastic leukemia. Leukemia,9, 1523-1533.
70. Wasserman, R., Galili, N., Ito, Y., Silber, J.H., Reichard, B.A., Shane, S., Womer, R.B., Lange, B. & Rovera, G. (1992) Residual disease at the end of induction therapy as a predictor of relapse during therapy in childhood B-lineage acute lymphoblastic leukemia. Journal of Clinical Oncology 10, 1879-1888.