Assessing a novel immuno-oncology-based combination therapy: Ipilimumab plus electrochemotherapy

References

• GLOBOCAN 2012: Estimated Cancer Incidence, Mortality and Prevalence Worldwide in 2012. http://globocan.iarc.fr/Default.aspx. Accessed 22 April 2014
   Google Scholar
• Robinson JK, Baker MK, Hillhouse JJ. New Approaches to Melanoma Prevention. Dermatol Clin 2012; 30: 405–12; PMID:22800548; http://dx.doi.org/10.1016/j.det.2012.04.006
   PubMedGoogle Scholar
• American Cancer Society Cancer Facts and Figures 2013. http://www.cancer.org/research/cancerfactsfigures/cancerfactsfigures/cancer-facts-figures-2013. Accessed 22 April 2014
   Google Scholar
• Krummel MF, Allison JP. CD28 and CTLA-4 have opposing effects on the response of T cells to stimulation. J Exp Med 1995; 182: 459–65; PMID:7543139; http://dx.doi.org/10.1084/jem.182.2.459
   PubMed Web of Science ®Google Scholar
• Blank C, Kuball J, Voelkl S, Wiendl H, Becker B, Walter B, Majdic O, Gajewski TF, Theobald M, Andreesen R et al. Blockade of PD-L1 (B7-H1) augments human tumor-specific T cell responses in vitro. Int J Cancer 2006; 119: 317–27; PMID:16482562; http://dx.doi.org/10.1002/ijc.21775
   PubMed Web of Science ®Google Scholar
• O'Day SJ, Hamid O, Urba WJ. Targeting cytotoxic T-lymphocyte antigen-4 (CTLA-4): a novel strategy for the treatment of melanoma and other malignancies. Cancer 2007; 110: 2614–27; PMID: 18000991; http://dx.doi.org/10.1002/cncr.23086
   PubMed Web of Science ®Google Scholar
• Lipson EJ, Drake CG. Ipilimumab: an anti-CTLA-4 antibody for metastatic melanoma. Clin Cancer Res 2011; 17: 6958–62; PMID:21900389; http://dx.doi.org/10.1158/1078-0432.CCR-11-1595
   PubMed Web of Science ®Google Scholar
• Hodi FS, O'Day SJ, McDermott DF, Weber RW, Sosman JA, Haanen JB, Gonzalez R, Robert C, Schadendorf D, Hassel JC et al. Improved survival with ipilimumab in patients with metastatic melanoma. N Engl J Med 2010; 363: 711–23; PMID:20525992; http://dx.doi.org/10.1056/NEJMoa1003466
   PubMed Web of Science ®Google Scholar
• Robert C, Thomas L, Bondarenko I, O'Day S, Weber J, Garbe C, Lebbe C, Baurain JF, Testori A, Grob JJ et al. Ipilimumab plus dacarbazine for previously untreated metastatic melanoma. N Engl J Med 2011; 364: 2517–26; PMID:21639810; http://dx.doi.org/10.1056/NEJMoa1104621
   PubMed Web of Science ®Google Scholar
• Wolchok JD, Kluger H, Callahan MK, Postow MA, Rizvi NA, Lesokhin AM, Segal NH, Ariyan CE, Gordon R-A, Reed K et al. Nivolumab plus ipilimumab in advanced melanoma. N Engl J Med 2013; 369: 122–33; PMID:23724867; http://dx.doi.org/10.1056/NEJMoa1302369
   PubMed Web of Science ®Google Scholar
• Sznol M, Kluger HM, Callahan MK, Postow MA, Gordon RA, Segal NH, Rizvi NA, Lesokhin AM, Atkins MB, Kirkwood JM et al. Survival, response duration, and activity by BRAF mutation (MT) status of nivolumab (NIVO, anti-PD-1, BMS-936558, ONO-4538) and ipilimumab (IPI) concurrent therapy in advanced melanoma (MEL). J Clin Oncol 2014; 32(Suppl. 5): abstract LBA9003ˆ
   Google Scholar
• Hiniker SM, Chen DS, Reddy S, Chang DT, Jones JC, Mollick JA, Swetter SM, Knox SJ. A systemic complete response of metastatic melanoma to local radiation and immunotherapy. Transl Oncol 2012; 5: 404–7; PMID:23323154; http://dx.doi.org/10.1593/tlo.12280
   PubMed Web of Science ®Google Scholar
• Postow MA, Callahan MK, Barker CA, Yamada Y, Yuan J, Kitano S, Mu Z, Rasalan T, Adamow M, Ritter E et al. Immunologic correlates of the abscopal effect in a patient with melanoma. N Engl J Med 2012; 366: 925–31; PMID:22397654; http://dx.doi.org/10.1056/NEJMoa1112824
   PubMed Web of Science ®Google Scholar
• Grimaldi AM, Simeone E, Giannarelli D, et al. Abscopal effects of radiotherapy on advanced melanoma patients who progressed after ipilimumab immunotherapy. Oncoimmunology 2014; 3:e28780; doi:10.4161/onci.28780
   Google Scholar
• Puzanov I, Milhem MM, Andtbacka RHI, Minor DR, Hamid O, Li A, Chastain M, Gorski K, Anderson A, Vanderwalde AM et al. Primary analysis of a phase 1b multicenter trial to evaluate safety and efficacy of talimogene laherparepvec (T-VEC) and ipilimumab (ipi) in previously untreated, unresected stage IIIB-IV melanoma. J Clin Oncol 2014; 32:5s, (suppl; abstr 9029ˆ); PMID:24190110; http://dx.doi.org/10.1200/JCO.2013.49.4757
   PubMed Web of Science ®Google Scholar
• Marty M, Sersa G, Garbay JR, Gehl J, Collins CG, Snoj M, Billard V, Geertsen PF, Larkin JO, Miklavcic D, et al. Electrochemotherapy - An easy, highly effective and safe treatment of cutaneous and subcutaneous metastases: Results of ESOPE (European Standard Operating Procedures of Electrochemotherapy) study. EJC Supplements 2006; 4: 3–13; http://dx.doi.org/10.1016/j.ejcsup.2006.08.002
   Web of Science ®Google Scholar
• Mir LM, Gehl J, Sersa G, Collins CG, Garbay J-R, Billard V, Geertsen PF, Rudolf Z, O'Sullivan GC, Marty M. Standard operating procedures of the electrochemotherapy: Instructions for the use of bleomycin or cisplatin administered either systemically or locally and electric pulses delivered by the CliniporatorTM by means of invasive or non-invasive electrodes. EJC Supplements 2006; 4: 14–25; http://dx.doi.org/10.1016/j.ejcsup.2006.08.003
   Web of Science ®Google Scholar
• Queirolo P, Marincola F, Spagnolo F. Electrochemotherapy for the management of melanoma skin metastasis: a review of the literature and possible combinations with immunotherapy. Arch Dermatol Res 2014; 306: 521–6; PMID:24682537; http://dx.doi.org/10.1007/s00403-014-1462-x
   PubMed Web of Science ®Google Scholar
• Mali B, Jarm T, Snoj M, Sersa G, Miklavcic D. Antitumor effectiveness of electrochemotherapy: a systematic review and meta-analysis. Eur J Surg Oncol 2013; 39: 4–16; PMID:22980492; http://dx.doi.org/10.1016/j.ejso.2012.08.016
   PubMed Web of Science ®Google Scholar
• Caracò C, Mozzillo N, Marone U, Simeone E, Benedetto L, Di Monta G, Di Cecilia ML, Botti G, Ascierto PA. Long-lasting response to electrochemotherapy in melanoma patients with cutaneous metastasis. BMC Cancer 2013; 13: 564; PMID: 24289268; http://dx.doi.org/10.1186/1471-2407-13-564
   PubMed Web of Science ®Google Scholar
• Campana LG, Valpione S, Mocellin S, Sundararajan R, Granziera E, Sartore L, Chiarion-Sileni V, Rossi CR. Electrochemotherapy for disseminated superficial metastases from malignant melanoma. Br J Surg 2012; 99: 821–30; PMID:22508342; http://dx.doi.org/10.1002/bjs.8749
   PubMed Web of Science ®Google Scholar
• Sersa G, Cemazar M, Menart V, Gaberc-Porekar V, Miklavcic D. Anti-tumor effectiveness of electrochemotherapy with bleomycin is increased by TNF-alpha on SA-1 tumors in mice. Cancer Lett 1997; 116: 85–92; PMID:9177462; http://dx.doi.org/10.1016/S0304-3835(97)00170-5
   PubMed Web of Science ®Google Scholar
• Mir LM, Orlowski S, Belehradek J Jr, Paoletti C. Electrochemotherapy potentiation of antitumour effect of bleomycin by local electric pulses. Eur J Cancer 1991; 27: 68–72; PMID:1707289; http://dx.doi.org/10.1016/0277-5379(91)90064-K
   PubMed Web of Science ®Google Scholar
• Mir LM, Orlowski S, Poddevin B, Belehradek J Jr. Electrochemotherapy tumor treatment is improved by interleukin-2 stimulation of the host's defences. Eur Cytokine Netw 1992; 3: 331–4; PMID:1379837
   PubMedGoogle Scholar
• Calvet CY, Famin D, André FM, Mir LM. Electrochemotherapy with bleomycin induces hallmarks of immunogenic cell death in murine colon cancer cells. OncoImmunology 2014; 3: e28131; PMID:25083316; http://dx.doi.org/10.4161/onci.28131
   PubMed Web of Science ®Google Scholar
• Simeone E, Gentilcore G, Giannarelli D, Grimaldi AM, Caracò C, Curvietto M, Esposito A, Paone M, Palla M, Cavalcanti E et al. Immunological and biological changes during ipilimumab treatment and their potential correlation with clinical response and survival in patients with advanced melanoma. Cancer Immunol Immunother 2014; 63:675–83; PMID:24695951; http://dx.doi.org/10.1007/s00262-014-1545-8
   PubMed Web of Science ®Google Scholar
• O'Day SJ, Maio M, Chiarion-Sileni V, Gajewski TF, Pehamberger H, Bondarenko IN, Queirolo P, Lundgren L, Mikhailov S, Roman L et al. Efficacy and safety of ipilimumab monotherapy in patients with pretreated advanced melanoma: a multicenter single-arm phase II study. Ann Oncol 2010; 21: 1712–7; PMID: 20147741; http://dx.doi.org/10.1093/annonc/mdq013
   PubMed Web of Science ®Google Scholar
• Queirolo P, Spagnolo F, Ascierto PA, Simeone E, Marchetti P, Scoppola A, Del Vecchio M, Di Guardo L, Maio M, Di Giacomo AM et al. Efficacy and safety of ipilimumab in patients with advanced melanoma and brain metastases. J Neurooncol 2014; 118: 109–16; PMID:24532241; http://dx.doi.org/10.1007/s11060-014-1400-y
   PubMed Web of Science ®Google Scholar
• Hersh EM, O'Day SJ, Powderly J, Khan KD, Pavlick AC, Cranmer LD, Samlowski WE, Nichol GM, Yellin MJ, Weber JS. A phase II multicenter study of ipilimumab with or without dacarbazine in chemotherapy-naïve patients with advanced melanoma. Invest New Drugs 2011; 29: 489–98; PMID:20082117; http://dx.doi.org/10.1007/s10637-009-9376-8
   PubMed Web of Science ®Google Scholar
• Di Giacomo AM, Ascierto PA, Pilla L, Santinami M, Ferrucci PF, Giannarelli D, Marasco A, Rivoltini L, Simeone E, Nicoletti SV et al. Ipilimumab and fotemustine in patients with advanced melanoma (NIBIT-M1): an open-label, single-arm phase 2 trial. Lancet Oncol 2012; 13: 879–86; PMID:22894884; http://dx.doi.org/10.1016/S1470-2045(12)70324-8
   PubMed Web of Science ®Google Scholar
• Burnette B, Fu Y-X, Weichselbaum RR. The confluence of radiotherapy and immunotherapy. Front Oncol 2012; 2: 143; PMID:23087904; http://dx.doi.org/10.3389/fonc.2012.00143
   PubMedGoogle Scholar
• Campana LG, Testori A, Mozzillo N, Rossi CR. Treatment of metastatic melanoma with electrochemotherapy. J Surg Oncol 2014; 109:301–7; PMID:24678530; http://dx.doi.org/10.1002/jso.23512
   PubMed Web of Science ®Google Scholar
• Gehl J, Anderson MH, Hastrup N, Straten PT, Geertsen PF. Electrochemotherapy with low-dose IL-2 in the treatment of disseminated malignant melanoma: clinical and paraclinical evidence of systemic immune response. Proc Am Soc Clin Oncol 2003; 22 ( abstract 2906)
   Google Scholar
• Gerlini G, Sestini S, Di Gennaro P, Urso C, Pimpinelli N, Borgognoni L. Dendritic cells recruitment in melanoma metastasis treated by electrochemotherapy. Clin Exp Metastasis 2013; 30: 37–45; PMID:22735940; http://dx.doi.org/10.1007/s10585-012-9505-1
   PubMed Web of Science ®Google Scholar
• Ku GY, Yuan J, Page DB, Schroeder SEA, Panageas KS, Carvajal RD, Chapman PB, Schwartz GK, Allison JP, Wolchok JD. Single-institution experience with ipilimumab in advanced melanoma patients in the compassionate use setting: lymphocyte count after 2 doses correlates with survival. Cancer 2010; 116: 1767–75; PMID:20143434; http://dx.doi.org/10.1002/cncr.24951
   PubMed Web of Science ®Google Scholar
• Liakou CI, Kamat A, Tang DN, Chen H, Sun J, Troncoso P, Logothetis C, Sharma P. CTLA-4 blockade increases IFNgamma-producing CD4+ICOShi cells to shift the ratio of effector to regulatory T cells in cancer patients. Proc Natl Acad Sci USA 2008; 105: 14987–92; PMID:18818309; http://dx.doi.org/10.1073/pnas.0806075105
   PubMed Web of Science ®Google Scholar
• Weber JS, Dummer R, de Pril V, Lebbé C, Hodi FS, MDX010-20 Investigators. Patterns of onset and resolution of immune-related adverse events of special interest with ipilimumab: detailed safety analysis from a phase 3 trial in patients with advanced melanoma. Cancer 2013; 119: 1675–82; PMID:23400564; http://dx.doi.org/10.1002/cncr.27969
   PubMed Web of Science ®Google Scholar
• Ascierto PA, Simeone E, Sileni VC, Pigozzo J, Maio M, Altomonte M, Del Vecchio M, Di Guardo L, Marchetti P, Ridolfi R et al. Clinical experience with ipilimumab 3 mg/kg: real-world efficacy and safety data from an expanded access programme cohort. J Transl Med 2014; 12: 116; PMID:24885479; http://dx.doi.org/10.1186/1479-5876-12-116
   PubMed Web of Science ®Google Scholar
• Matthiessen LW, Chalmers RL, Sainsbury DC, Veeramani S, Kessell G, Humphreys AC, Bond JE, Muir T, Gehl J. Management of cutaneous metastases using electrochemotherapy. Acta Oncol 2011; 50: 621–9; PMID:21574833; http://dx.doi.org/10.3109/0284186X.2011.573626
   PubMed Web of Science ®Google Scholar
• Wolchok JD, Hoos A, O'Day S, Weber JS, Hamid O, Lebbé C, Maio M, Binder M, Bohnsack, O, Nichol G et al. Guidelines for the evaluation of immune therapy activity in solid tumors: immune-related response criteria. Clin Cancer Res 2009; 15: 7412–20; PMID:19934295; http://dx.doi.org/10.1158/1078-0432.CCR-09-1624
   PubMed Web of Science ®Google Scholar
• Del Vecchio M, Di Guardo L, Ascierto PA, Grimaldi AM, Sileni VC, Pigozzo J, Ferraresi V, Nuzzo C, Rinaldi G, Testori A et al. Efficacy and safety of ipilimumab 3mg/kg in patients with pretreated, metastatic, mucosal melanoma. Eur J Cancer 2014; 50: 121–7; PMID:24100024; http://dx.doi.org/10.1016/j.ejca.2013.09.007
   PubMed Web of Science ®Google Scholar
• Di Giacomo AM, Danielli R, Calabrò L, Bertocci E, Nannicini C, Giannarelli D, Balestrazzi A, Vigni F, Riversi V, Miracco C et al. Ipilimumab experience in heavily pretreated patients with melanoma in an expanded access program at the University Hospital of Siena (Italy). Cancer Immunol Immunother 2011; 60: 467–77; PMID:21170646; http://dx.doi.org/10.1007/s00262-010-0958-2
   PubMed Web of Science ®Google Scholar
• Di Giacomo AM, Calabrò L, Danielli R, Fonsatti E, Bertocci E, Pesce I, Fazio C, Cutaia O, Giannarelli D, Miracco C et al. Long-term survival and immunological parameters in metastatic melanoma patients who responded to ipilimumab 10 mg/kg within an expanded access programme. Cancer Immunol Immunother 2013; 62: 1021–8; PMID:23591982; http://dx.doi.org/10.1007/s00262-013-1418-6
   PubMed Web of Science ®Google Scholar
• Queirolo P, Simeone E, De Galitiis F, Di Guardo L, Marconcini R, Di Giacomo AM, Ferraresi V, De Rosa F, Guida Stragliotto MS. Efficacy and safety data from patients with advanced melanoma and brain metastases participating in the European ipilimumab expanded access programme (EAP) in Italy. Ann Oncol 2012; 23 (suppl. 9), ix369 ( abstract 1132)
   Google Scholar