Treatment of acute promyelocytic leukemia with arsenic trioxide: clinical results and open questions

References

• The International Agency for Research on Cancer. WHO classification of tumours of haemopoietic and lymphoid tissues. WHO Press, Lyon 112–114 (2008).
   Google Scholar
• Rowley JD, Golomb H, Dougherty C. 15/17 Translocation, a consistent chromosomal change in acute promyelocytic leukemia. Lancet 1(8010), 549–550 (1977).
   PubMed Web of Science ®Google Scholar
• De The H, Chomienne C, Lanotte M, Degos L, Dejean A. The t(15;17) translocation of acute promyelocytic leukemia fuses the retinoic acid receptor α gene to a novel transcribed locus. Nature 347(6293), 588–561 (1990).
   Google Scholar
• Kakizuka A, Miller WH, Umesono K et al. Chromosomal translocation t(15;17) in human acute promyelocytic leukemia fuses RARa with a novel putative transcription factor, PML. Cell 66(4), 663–674 (1991).
   PubMed Web of Science ®Google Scholar
• Alcalay M, Zangrilli D, Fagioli M et al. Expression pattern of the RARa fusion gene in acute promyelocytic leukemia. Proc. Natl Acad. Sci. USA 89(11), 4840–4844 (1992).
   PubMed Web of Science ®Google Scholar
• Lengfelder E, Saussele S, Weisser A, Büchner T, Hehlmann R. Treatment concepts of acute promyelocytic leukemia. Crit. Rev. Oncol. Hematol. 56(2), 261–274 (2005).
   PubMed Web of Science ®Google Scholar
• Tallman MS, Kwaan HC. Reassessing the hemostatic disorder associated with acute promyelocytic leukemia. Blood 79(3), 543–553 (1992).
   PubMed Web of Science ®Google Scholar
• Yanada M, Matsushita T, Asou N et al. Severe hemorrhagic complications during remission induction therapy for acute promyelocytic leukemia: incidence, risk factors and influence on outcome. Eur. J. Haematol. 78(3), 213–219 (2007).
   PubMed Web of Science ®Google Scholar
• Sanz MA, Lo-Coco F, Martin G et al. Definition of relapse risk and role of non-anthracycline drugs for consolidation in patients with acute promyelocytic leukemia: a joint study of the PETHEMA and GIMEMA cooperative groups. Blood 96(4), 1247–1252 (2000).
   PubMed Web of Science ®Google Scholar
• De la Serna J, Montesinos P, Vellenga E et al. Causes and prognostic factors of remission induction failure in patients with acute promyelocytic leukemia treated with all-trans retinoic acid and idarubicin. Blood 111(7), 3395–3402 (2008).
   PubMed Web of Science ®Google Scholar
• Gale RE, Hills R, Pizzey AR et al. Relationship between FLT3 mutation status, biologic characteristics, and response to targeted therapy in acute ptomyelocytic leukemia. Blood 106(12), 3768–3776 (2005).
   PubMedGoogle Scholar
• Montesinos P, Rayón C, Vellenga E et al. Clinical significance of CD56 expression in patients with acute promyelocytic leukemia treated with all-trans retinoic acid and anthracycline-based regimens. Blood 117(6), 1799–1805 (2011).
   PubMed Web of Science ®Google Scholar
• Schnittger S, Bacher U, Haferlach C, Kern W, Alpermann T, Haferlach T. Clinical impact of FLT3 mutation load in acute promyelocytic leukemia with t(15;17)/PML-RARA. Haematologica 96(12), 1799–1807 (2011).
   PubMedGoogle Scholar
• Bernard J, Weil M, Boiron M, Jacquillat C, Flandrin G, Gemon MF. Acute promyelocytic leukemia: results of treatment by daunorubicin. Blood 41(4), 489–496 (1973).
   PubMed Web of Science ®Google Scholar
• Huang M, Ye Y, Chen S et al. Use of all-trans retinoic acid in the treatment of acute promyelocytic leukemia. Blood 72(2), 567–572 (1988).
   PubMed Web of Science ®Google Scholar
• Shen ZX, Chen GQ, Ni JH et al. Use of arsenic trioxide (As2O3) in the treatment of acute promyelocytic leukemia (APL): II. Clinical efficacy and pharmacokinetics in relapsed patients. Blood 89(9), 3354–3360 (1997).
   PubMed Web of Science ®Google Scholar
• Sanz MA, Grimwade D, Tallman MS et al. Management of acute promyelocytic leukemia: Recommendations from an expert panel on behalf of the European Leukemia Net. Blood 113(9), 1875–1891 (2009).
   PubMed Web of Science ®Google Scholar
• Wang ZY, Chen Z. Acute promyelocytic leukemia: from highly fatal to highly curable. Blood 111(5), 2505–2515 (2008).
   PubMed Web of Science ®Google Scholar
• Lehmann S, Ravn A, Carlsson L et al. Continuing high early death rate in acute promyelocytic leukemia: a population-based report from the Swedish Adult Acute Leukemia Registry. Leukemia 25(7), 1128–1134 (2011).
   PubMed Web of Science ®Google Scholar
• Lengfelder E, Hanfstein B, Haferlach et al. Outcome of elderly patients with acute promyelocytic leukemia: results of the German Acute Myeloid Leukemia Cooperative Group. Ann. Hematol. 92(1), 41–52 (2013).
   PubMed Web of Science ®Google Scholar
• McClellan JS, Kohrt HE, Coutre S et al. Treatment advances have not improved the early death rate in acute promyelocytic leukemia. Haematologica 97(1), 133–136 (2012).
   PubMed Web of Science ®Google Scholar
• Diverio D, Rossi V, Avvisati G et al. Early detection of relapse by prospective reverse transcriptase-polymerase chain reaction analysis of the PML/RARα fusion gene in patients with acute promyelocytic leukemia enrolled in the GIMEMA-AIEOP multicenter ‘AIDA’ trial. Blood 92(3), 784–789 (1998).
   PubMed Web of Science ®Google Scholar
• Adès L, Guerci A, Raffoux E et al. Very long-term outcome of acute promyelocytic leukemia after treatment with all-trans retinoic acid and chemotherapy: the European APL Group experience. Blood 115(9), 1690–1696 (2010).
   PubMed Web of Science ®Google Scholar
• Tallman MS, Andersen JW, Schiffer CA et al. All-trans retinoic acid in acute promyelocytic leukemia: long-term outcome and prognostic factor analysis from the North American Intergroup protocol. Blood 100(13), 4298–4302 (2002).
   PubMed Web of Science ®Google Scholar
• Estey E, Garcia-Manero G, Ferrajoli et al. Use of all-trans retinoic acid plus arsenic trioxide as an alternative to chemotherapy in untreated acute promyelocytic leukemia. Blood 107(9), 3469–3473 (2006).
   PubMed Web of Science ®Google Scholar
• Mathews V, George B, Chendamarai E et al. Single-agent arsenic trioxide in the treatment of newly diagnosed acute promyelocytic leukemia: long-term follow-up data. J. Clin. Oncol. 28(24), 3866–3871 (2010).
   PubMed Web of Science ®Google Scholar
• Ghavamzadeh A, Alimoghaddam K, Rostami S et al. Phase II study of single-agent arsenic trioxide for the front-line therapy of acute promyelocytic leukemia. J. Clin. Oncol. 29(20), 2753–2757 (2011).
   PubMed Web of Science ®Google Scholar
• Lo-Coco F, Avvisati G, Vignetti M et al. Retinoic acid and arsenic trioxide for acute promyelocytic leukemia. N. Engl. J. Med. 369(2), 111–121 (2013).
   PubMed Web of Science ®Google Scholar
• Melnick A, Licht JD. Deconstructing a disease: RARalpha, its fusion partners, and their roles in the pathogenesis of acute promyelocytic leukemia. Blood 93(10), 3167–3215 (1999).
   PubMed Web of Science ®Google Scholar
• Zhu J, Lallemand-Breitenbach V, de Thé H. Pathways of retinoic acid- or arsenic trioxide-induced PML/RARalpha catabolism, role of oncogene degradation in disease remission. Oncogene 20(49), 7257–7265 (2001).
   PubMedGoogle Scholar
• He LZ, Tribioli C, Rivi R et al. Acute leukemia with promyelocytic features in PML/RARalpha transgenic mice. Proc. Natl Acad. Sci. USA 94(10), 5302–5307 (1997).
   PubMed Web of Science ®Google Scholar
• Ablain J, de The H. Revisiting the differentiation paradigm in acute promyelocytic leukemia. Blood 117(22), 5795–5802 (2011).
   PubMedGoogle Scholar
• Miller WH Jr, Schipper HM, Lee JS, Singer J, Waxman S. Mechanisms of action of arsenic trioxide. Cancer Res. 62(14), 3893–3903 (2002).
   PubMed Web of Science ®Google Scholar
• Chen GQ, Shi XG, Tang W et al. Use of arsenic trioxide (As2O3) in the treatment of acute promyelocytic leukemia (APL): I. As2O3 exerts dose-dependent dual effects on APL cells. Blood 89(9), 3345–3353 (1997).
   PubMed Web of Science ®Google Scholar
• Zhu J, Koken MH, Quignon F et al. Arsenic-induced PML targeting onto nuclear bodies: implications for the treatment of acute promyelocytic leukemia. Proc. Natl Acad Sci. USA 94(8), 3978–3983 (1997).
   PubMed Web of Science ®Google Scholar
• Chou WC, Hawkins AL, Barrett JF, Griffin CA, Dang CV. Arsenic inhibition of telomerase transcription leads to genetic instability. J. Clin. Invest. 108(10), 1541–1547 (2001).
   PubMedGoogle Scholar
• Lallemand-Breitenbach V, Guillemin MC, Janin A et al. Retinoic acid and arsenic synergize to eradicate leukemic cells in a mouse model of acute promyelocytic leukemia. J. Exp. Med. 189(7), 1043–1053 (1999).
   PubMed Web of Science ®Google Scholar
• Shen ZX, Shi ZZ, Fang J et al. All-trans retinoic acid/As2O3 combination yields a high quality remission and survival in newly diagnosed acute promyelocytic leukemia. Proc. Natl Acad. Sci. USA 101(15), 5328–5335 (2004).
   PubMed Web of Science ®Google Scholar
• Zhu J, Kopf E, Honoré N et al. Retinoic acid induces proteasome-dependent degradation of retinoic acid receptor alpha (RARalpha) and oncogenic RARalpha fusion proteins. Proc. Natl Acad. Sci. USA 96(26), 14807–14812 (1999).
   PubMed Web of Science ®Google Scholar
• Zhang XW, Yan XJ, Zhou ZR et al. Arsenic trioxide controls the fate of the PML-RARalpha oncoprotein by directly binding PML. Science 328(5975), 240–243 (2010).
   PubMed Web of Science ®Google Scholar
• Fujisawa S, Ohno R, Shigeno K et al. Pharmacokinetics of arsenic species in Japanese patients with relapsed or refractory acute promyelocytic leukemia treated with arsenic trioxide. Cancer Chemother. Pharmacol. 59(4), 485–493 (2007).
   PubMed Web of Science ®Google Scholar
• Au WY, Tam S, Fong BM, Kwong YL. Elemental arsenic entered the cerebrospinal fluid during oral arsenic trioxide treatment of meningeal relapse of acute promyelocytic leukemia. Blood 107(7), 3012–3013 (2006).
   PubMedGoogle Scholar
• Lengfelder E, Hofmann WK, Nowak D. Impact of arsenic trioxide in the treatment of acute promyelocytic leukemia. Leukemia 26(3), 433–442 (2012).
   PubMed Web of Science ®Google Scholar
• Ravandi F, Estey E, Jones D et al. Effective treatment of acute promyelocytic leukemia with all-trans-retinoic acid, arsenic trioxide, and gemtuzumab ozogamicin. J. Clin. Oncol. 27(4), 504–510 (2009).
   PubMed Web of Science ®Google Scholar
• Zhang Y, Zhang Z, Li J et al. Long-term efficacy and safety of arsenic trioxide for first-line treatment of elderly patients with newly diagnosed acute promyelocytic leukemia. Cancer 119(1), 115–125 (2012).
   PubMedGoogle Scholar
• Hu J, Liu YF, Wu CF, Xu F et al. Long-term efficacy and safety of all-trans retinoic acid/arsenic trioxide-based therapy in newly diagnosed acute promyelocytic leukemia. Proc. Natl Acad. Sci. USA 106(9), 3342–3347 (2009).
   PubMed Web of Science ®Google Scholar
• Powell BL, Moser B, Stock W et al. Arsenic trioxide improves event-free and overall survival for adults with acute promyelocytic leukemia: North American Leukemia Intergroup Study C9710. Blood 116(19), 3751–3757 (2010).
   PubMed Web of Science ®Google Scholar
• Gore SD, Gojo I, Sekeres MA et al. Single cycle of arsenic trioxide-based consolidation chemotherapy spares anthracycline exposure in the primary management of acute promyelocytic leukemia. J. Clin. Oncol. 28(6), 1047–1053 (2010).
   PubMed Web of Science ®Google Scholar
• Iland HJ, Bradstock K, Supple et al. All-trans-retinoic acid, idarubicin, and IV arsenic trioxide as initial therapy in acute promyelocytic leukemia (APML4). Blood 120(8), 1570–1580 (2012).
   PubMed Web of Science ®Google Scholar
• Ades L, Raffoux E, Chevret S et al. Arsenic Trioxide (ATO) in the consolidation treatment of newly diagnosed apl-first interim analysis of a randomized trial (APL 2006) by the French Belgian Swiss APL Group. Presented at: 52th ASH Annual Meeting. Orlando, FL, USA, 4–7 December 2010.
   Google Scholar
• Lu DP, Qiu JY, Wang Q et al. Tetra-arsenic tetra-sulfide for the treatment of acute promyelocytic leukemia: A pilot report. Blood 99(9), 3136–3143 (2002).
   PubMed Web of Science ®Google Scholar
• Au WV, Kumana CR, Lee HK et al. Oral arsenic trioxide-based maintenance regimens for first complete remission of acute promyelocytic leukemia: a 10-year follow-up study. Blood 118(25), 6535–6543 (2011).
   PubMed Web of Science ®Google Scholar
• Zhang P, Wang S, Hu L et al. Seven years' summary report on the treatment of acute promyelocytic leukemia with arsenic trioxide--an analysis of 242 cases. Zhonghua Xue Ye Xue Za Zhi 21(2), 67–70 (2000).
   PubMedGoogle Scholar
• Soignet SL, Frankel SR, Douer D et al. United States multicenter study of arsenic trioxide in relapsed acute promyelocytic leukemia. J. Clin. Oncol. 19(18), 3852–3860 (2001).
   PubMed Web of Science ®Google Scholar
• Grimwade D, Jovanovic JV, Hills RK et al. Prospective minimal residual disease monitoring to predict relapse of acute promyelocytic leukemia and to direct pre-emptive arsenic trioxide therapy. J. Clin. Oncol. 27(22), 3650–3658 (2009).
   PubMed Web of Science ®Google Scholar
• Niu C, Yan H, Yu T et al. Studies on treatment of acute promyelocytic leukemia with arsenic trioxide: remission induction, follow-up, and molecular monitoring in 11 newly diagnosed and 47 relapsed acute promyelocytic leukemia patients. Blood 94(10), 3315–3324 (1999).
   PubMed Web of Science ®Google Scholar
• Douer D, Tallman MS. Arsenic trioxide: new clinical experience with an old medication in hematologic malignancies. J. Clin. Oncol. 23(10), 2396–2410 (2005).
   PubMedGoogle Scholar
• Douer D, Hu W, Giralt S, Lill M, DiPersio J. Arsenic trioxide (trisenox) therapy for acute promyelocytic leukemia in the setting of hematopoietic stem cell transplantation. Oncologist 8(2), 132–140 (2003).
   PubMedGoogle Scholar
• Thomas X, Pigneux A, Raffoux E, Huguet F, Caillot D, Fenaux P. Superiority of an arsenic trioxide-based regimen over a historic control combining all-trans retinoic acid plus intensive chemotherapy in the treatment of relapsed acute promyelocytic leukemia. Haematologica 91(7), 996–997 (2006).
   PubMed Web of Science ®Google Scholar
• Thirugnanam R, George B, Chendamarai E et al. Comparison of clinical outcomes of patients with relapsed acute promyelocytic leukemia induced with arsenic trioxide and consolidated with either an autologous stem cell transplant or an arsenic trioxide-based regimen. Biol. Blood Marrow Transplant. 15(11), 1479–1484 (2009).
   PubMed Web of Science ®Google Scholar
• Yanada M, Tsuzuki M, Fujita H et al. Phase 2 study of arsenic trioxide followed by autologous hematopoietic cell transplantation for relapsed acute promyelocytic leukemia. Blood 121(16), 3095–3102 (2013).
   PubMed Web of Science ®Google Scholar
• Au W, Lie A, Chim C et al. Arsenic trioxide in comparison with chemotherapy and bone marrow transplantation for the treatment of relapsed acute promyelocytic leukaemia. Ann. Oncol. 14(5), 752–757 (2003).
   PubMedGoogle Scholar
• Ramadan SM, Di Veroli A, Camboni A et al. Allogeneic stem cell transplantation for advanced acute promyelocytic leukemia in the ATRA and ATO era. Haematologica 97(11), 1731–1735 (2012).
   PubMed Web of Science ®Google Scholar
• De Botton S, Sanz MA, Chevret S et al. Extramedullary relapse in acute promyelocytic leukemia treated with all-trans retinoic acid and chemotherapy. Leukemia 20(1), 35–41 (2006).
   PubMed Web of Science ®Google Scholar
• Camacho LH, Soignet SL, Chanel S et al. Leukocytosis and the retinoic acid syndrome in patients with acute promyelocytic leukemia treated with arsenic trioxide. J. Clin. Oncol. 18(13), 2620–2625 (2000).
   PubMed Web of Science ®Google Scholar
• Mathews V, Thomas M, Srivastava VM, George B, Srivastava A, Chandy M. Impact of FLT3 mutations and secondary cytogenetic changes on the outcome of patients with newly diagnosed acute promyelocytic leukemia treated with a single agent arsenic trioxide regimen. Haematologica 92(7), 994–995 (2007).
   PubMedGoogle Scholar
• Chendamarai E, Balasubramanian P, George B et al. Role of minimal residual disease monitoring in acute promyelocytic leukemia treated with arsenic trioxide in frontline therapy. Blood 119(15), 3413–3419 (2012).
   PubMed Web of Science ®Google Scholar
• Ferrara F, Finizio O, D'Arco A, Mastrullo L, Cantore N, Musto P. Acute promyelocytic leukemia in patients aged over 60 years: multicenter experience of 34 consecutive unselected patients. Anticancer Res. 30(3), 967–971 (2010).
   PubMed Web of Science ®Google Scholar
• Adès L, Sanz MA, Chevret S et al. Treatment of newly diagnosed acute promyelocytic leukemia (APL): a comparison of French-Belgian-Swiss and PETHEMA results. Blood 111(3), 1078–1084 (2008).
   PubMedGoogle Scholar
• Lengfelder E, Haferlach C, Saussele S et al. High dose ara-C in the treatment of newly diagnosed acute promyelocytic leukemia: long-term results of the German AMLCG. Leukemia 23(12), 2248–2258 (2009).
   PubMedGoogle Scholar
• Sanz MA, Montesinos P, Rayón C et al. Risk-adapted treatment of acute promyelocytic leukemia based on all-trans retinoic acid and anthracycline with addition of cytarabine in consolidation therapy for high-risk patients: further improvements in treatment outcome. Blood 115(25), 5137–5146 (2010).
   PubMed Web of Science ®Google Scholar
• Lo-Coco F, Avvisati G, Vignetti M et al. Front-line treatment of acute promyelocytic leukemia with AIDA induction followed by risk-adapted consolidation for adults younger than 61 years: results of the AIDA-2000 trial of the GIMEMA Group. Blood 116(17), 3171–3179 (2010).
   PubMed Web of Science ®Google Scholar
• Soignet SL, Maslak P, Wang ZG et al. Complete remission after treatment of acute promyelocytic leukemia with arsenic trioxide. N. Engl. J. Med. 339(19), 1341–1348 (1998).
   PubMed Web of Science ®Google Scholar
• Shigeno K, Naito K, Sahara N et al. Arsenic trioxide therapy in relapsed or refractory Japanese patients with acute promyelocytic leukemia: updated outcomes of the phase II study and postremission therapies. Int. J. Hematol. 82(3), 224–229 (2005).
   PubMed Web of Science ®Google Scholar
• Alimoghaddam K, Ghavamzadeh A, Jahani M et al. Treatment of relapsed acute promyelocytic leukemia by arsenic trioxide in Iran. Arch. Iran. Med. 14(3), 167–169 (2011).
   PubMed Web of Science ®Google Scholar