Regression of Metastatic Renal-Cell Carcinoma after Nonmyeloablative Allogeneic Peripheral-Blood Stem-Cell Transplantation
Richard Childs, M.D., Allen Chernoff, M.D., Nathalie Contentin, M.D., Erkut Bahceci, M.D., David Schrump, M.D., Susan Leitman, M.D., Elizabeth J. Read, M.D., John Tisdale, M.D., Cynthia Dunbar, M.D., W. Marston Linehan, M.D., Neal S. Young, M.D., and A. John Barrett, M.D.
Background Since allogeneic stem-cell transplantation can inducecurative graft-versus-leukemia reactions in patients with hematologiccancers, we sought to induce analogous graft-versus-tumor effectsin patients with metastatic renal-cell carcinoma by means ofnonmyeloablative allogeneic peripheral-blood stem-cell transplantation.
Methods Nineteen consecutive patients with refractory metastaticrenal-cell carcinoma who had suitable donors received a preparativeregimen of cyclophosphamide and fludarabine, followed by aninfusion of a peripheral-blood stem-cell allograft from an HLA-identicalsibling or a sibling with a mismatch of a single HLA antigen.Cyclosporine, used to prevent graft-versus-host disease, waswithdrawn early in patients with mixed T-cell chimerism or diseaseprogression. Patients with no response received up to threeinfusions of donor lymphocytes.
Results At the time of the last follow-up, 9 of the 19 patientswere alive 287 to 831 days after transplantation (median follow-up,402 days). Two had died of transplantation-related causes, andeight from progressive disease. In 10 patients (53 percent)metastatic disease regressed; 3 had a complete response, and7 had a partial response. The patients who had a complete responseremained in remission 27, 25, and 16 months after transplantation.Regression of metastases was delayed, occurring a median of129 days after transplantation, and often followed the withdrawalof cyclosporine and the establishment of complete donor–T-cellchimerism. These results are consistent with a graft-versus-tumoreffect.
Conclusions Nonmyeloablative allogeneic stem-cell transplantationcan induce sustained regression of metastatic renal-cell carcinomain patients who have had no response to conventional immunotherapy.
Source Information
From the Hematology Branch, National Heart, Lung, and Blood Institute (R.C., N.C., E.B., C.D., N.S.Y., A.J.B.); the Urologic Oncology Branch (A.C., W.M.L.) and the Surgery Branch (D.S.), Division of Clinical Sciences, National Cancer Institute; the Department of Transfusion Medicine, Warren Grant Magnuson Clinical Center (S.L., E.J.R.), and the Molecular and Clinical Hematology Branch (J.T.), National Institute of Diabetes and Digestive and Kidney Diseases — all at the National Institutes of Health, Bethesda, Md. Other authors were Emmanuel Clave, Ph.D., Diane Epperson, Ph.D., and Virginia Mayo, R.N., Hematology Branch, National Heart, Lung, and Blood Institute, National Institutes of Health, Bethesda, Md.
Address reprint requests to Dr. Childs at the Hematology Branch, NHLBI/NIH, 10/7C103, 10 Center Dr., M.S.C. 1652, Bethesda, MD 20892-1652, or at childsr{at}nih.gov.
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Curti, B. D.
(2004). Renal Cell Carcinoma. JAMA
292: 97-100
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Igarashi, T., Wynberg, J., Srinivasan, R., Becknell, B., McCoy, J. P. Jr, Takahashi, Y., Suffredini, D. A., Linehan, W. M., Caligiuri, M. A., Childs, R. W.
(2004). Enhanced cytotoxicity of allogeneic NK cells with killer immunoglobulin-like receptor ligand incompatibility against melanoma and renal cell carcinoma cells. Blood
104: 170-177
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Negrier, S., Perol, D., Menetrier-Caux, C., Escudier, B., Pallardy, M., Ravaud, A., Douillard, J.-Y., Chevreau, C., Lasset, C., Blay, J.-Y.
(2004). Interleukin-6, Interleukin-10, and Vascular Endothelial Growth Factor in Metastatic Renal Cell Carcinoma: Prognostic Value of Interleukin-6--From the Groupe Francais d'Immunotherapie. JCO
22: 2371-2378
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Miyakoshi, S., Yuji, K., Kami, M., Kusumi, E., Kishi, Y., Kobayashi, K., Murashige, N., Hamaki, T., Kim, S.-W., Ueyama, J.-i., Mori, S.-i., Morinaga, S.-i., Muto, Y., Masuo, S., Kanemaru, M., Hayashi, T., Takaue, Y., Taniguchi, S.
(2004). Successful Engraftment After Reduced-Intensity Umbilical Cord Blood Transplantation for Adult Patients with Advanced Hematological Diseases. Clin. Cancer Res.
10: 3586-3592
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Griffiths, T R L, Mellon, J K
(2004). Evolving immunotherapeutic strategies in bladder and renal cancer. Postgrad. Med. J.
80: 320-327
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Matte, C. C., Cormier, J., Anderson, B. E., Athanasiadis, I., Liu, J., Emerson, S. G., Pear, W., Shlomchik, W. D.
(2004). Graft-versus-leukemia in a retrovirally induced murine CML model: mechanisms of T-cell killing. Blood
103: 4353-4361
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Childs, R. W.
(2004). Evolving trends in hematopoietic cell transplantation for solid tumors: tempering enthusiasm with clinical reality. Ann Oncol
15: 543-544
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Mapara, M. Y., Sykes, M.
(2004). Tolerance and Cancer: Mechanisms of Tumor Evasion and Strategies for Breaking Tolerance. JCO
22: 1136-1151
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Atkins, M. B., Hidalgo, M., Stadler, W. M., Logan, T. F., Dutcher, J. P., Hudes, G. R., Park, Y., Liou, S.-H., Marshall, B., Boni, J. P., Dukart, G., Sherman, M. L.
(2004). Randomized Phase II Study of Multiple Dose Levels of CCI-779, a Novel Mammalian Target of Rapamycin Kinase Inhibitor, in Patients With Advanced Refractory Renal Cell Carcinoma. JCO
22: 909-918
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Takahashi, Y., McCoy, J. P. Jr, Carvallo, C., Rivera, C., Igarashi, T., Srinivasan, R., Young, N. S., Childs, R. W.
(2004). In vitro and in vivo evidence of PNH cell sensitivity to immune attack after nonmyeloablative allogeneic hematopoietic cell transplantation. Blood
103: 1383-1390
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Carvallo, C., Geller, N., Kurlander, R., Srinivasan, R., Mena, O., Igarashi, T., Griffith, L. M., Linehan, W. M., Childs, R. W.
(2004). Prior chemotherapy and allograft CD34+ dose impact donor engraftment following nonmyeloablative allogeneic stem cell transplantation in patients with solid tumors. Blood
103: 1560-1563
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Kolb, H.-J., Schmid, C., Barrett, A. J., Schendel, D. J.
(2004). Graft-versus-leukemia reactions in allogeneic chimeras. Blood
103: 767-776
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Blaise, D., Bay, J. O., Faucher, C., Michallet, M., Boiron, J.-M., Choufi, B., Cahn, J.-Y., Gratecos, N., Sotto, J.-J., Francois, S., Fleury, J., Mohty, M., Chabannon, C., Bilger, K., Gravis, G., Viret, F., Braud, A. C., Bardou, V. J., Maraninchi, D., Viens, P.
(2004). Reduced-intensity preparative regimen and allogeneic stem cell transplantation for advanced solid tumors. Blood
103: 435-441
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Butterfield, L. H., Ribas, A., Meng, W. S., Dissette, V. B., Amarnani, S., Vu, H. T., Seja, E., Todd, K., Glaspy, J. A., McBride, W. H., Economou, J. S.
(2003). T-Cell Responses to HLA-A*0201 Immunodominant Peptides Derived from {alpha}-Fetoprotein in Patients with Hepatocellular Cancer. Clin. Cancer Res.
9: 5902-5908
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Young, K. J., Kay, L. S., Phillips, M. J., Zhang, L.
(2003). Antitumor Activity Mediated by Double-Negative T Cells. Cancer Res.
63: 8014-8021
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Ueno, N. T., Cheng, Y. C., Rondon, G., Tannir, N. M., Gajewski, J. L., Couriel, D. R., Hosing, C., de Lima, M. J., Anderlini, P., Khouri, I. F., Booser, D. J., Hortobagyi, G. N., Pagliaro, L. C., Jonasch, E., Giralt, S. A., Champlin, R. E.
(2003). Rapid induction of complete donor chimerism by the use of a reduced-intensity conditioning regimen composed of fludarabine and melphalan in allogeneic stem cell transplantation for metastatic solid tumors. Blood
102: 3829-3836
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Sosman, J. A.
(2003). Targeting of the VHL-Hypoxia-Inducible Factor-Hypoxia-Induced Gene Pathway for Renal Cell Carcinoma Therapy. J. Am. Soc. Nephrol.
14: 2695-2702
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Strair, R. K., Schaar, D., Medina, D., Todd, M. B., Aisner, J., DiPaola, R. S., Manago, J., Knox, B., Jenkinson, A., Senzon, R., Baker, C., Dudek, L., Ciardella, M., Kuriyan, M., Rubin, A., Lattime, E. C.
(2003). Antineoplastic Effects of Partially HLA-Matched Irradiated Blood Mononuclear Cells in Patients With Renal Cell Carcinoma. JCO
21: 3785-3791
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Pantuck, A. J., Zeng, G., Belldegrun, A. S., Figlin, R. A.
(2003). Pathobiology, Prognosis, and Targeted Therapy for Renal Cell Carcinoma: Exploiting the Hypoxia-Induced Pathway. Clin. Cancer Res.
9: 4641-4652
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Fukuda, T., Hackman, R. C., Guthrie, K. A., Sandmaier, B. M., Boeckh, M., Maris, M. B., Maloney, D. G., Deeg, H. J., Martin, P. J., Storb, R. F., Madtes, D. K.
(2003). Risks and outcomes of idiopathic pneumonia syndrome after nonmyeloablative and conventional conditioning regimens for allogeneic hematopoietic stem cell transplantation. Blood
102: 2777-2785
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Barker, J. N., Weisdorf, D. J., DeFor, T. E., Blazar, B. R., Miller, J. S., Wagner, J. E.
(2003). Rapid and complete donor chimerism in adult recipients of unrelated donor umbilical cord blood transplantation after reduced-intensity conditioning. Blood
102: 1915-1919
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Renga, M., Pedrazzoli, P., Siena, S.
(2003). Present results and perspectives of allogeneic non-myeloablative hematopoietic stem cell transplantation for treatment of human solid tumors. Ann Oncol
14: 1177-1184
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Fukuda, T., Boeckh, M., Carter, R. A., Sandmaier, B. M., Maris, M. B., Maloney, D. G., Martin, P. J., Storb, R. F., Marr, K. A.
(2003). Risks and outcomes of invasive fungal infections in recipients of allogeneic hematopoietic stem cell transplants after nonmyeloablative conditioning. Blood
102: 827-833
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Mohty, M., Bay, J.-O., Faucher, C., Choufi, B., Bilger, K., Tournilhac, O., Vey, N., Stoppa, A.-M., Coso, D., Chabannon, C., Viens, P., Maraninchi, D., Blaise, D.
(2003). Graft-versus-host disease following allogeneic transplantation from HLA-identical sibling with antithymocyte globulin-based reduced-intensity preparative regimen. Blood
102: 470-476
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Ribas, A., Butterfield, L. H., Glaspy, J. A., Economou, J. S.
(2003). Current Developments in Cancer Vaccines and Cellular Immunotherapy. JCO
21: 2415-2432
[Abstract][Full Text]
