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Journal of Drug Delivery
Volume 2013 (2013), Article ID 456409, 12 pages
http://dx.doi.org/10.1155/2013/456409
Review Article

Liposomal Doxorubicin in the Treatment of Breast Cancer Patients: A Review

1Medical Oncology Department, Miguel Servet University Hospital, Paseo Isabel la Católica, 1-3, 50009 Zaragoza, Spain
2Aragón Institute of Health Sciences, Avda. San Juan Bosco, 13, planta 1, 50009 Zaragoza, Spain

Received 1 December 2012; Accepted 10 February 2013

Academic Editor: Michele Caraglia

Copyright © 2013 Juan Lao et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. D. R. Khan, E. M. Rezler, J. Lauer-Fields, and G. B. Fields, “Effects of drug hydrophobicity on liposomal stability,” Chemical Biology and Drug Design, vol. 71, no. 1, pp. 3–7, 2008. View at Publisher · View at Google Scholar · View at Scopus
  2. New RRC, Liposomes: A Practical Approach, Oxford University Press, Oxford, UK, 1st edition, 1990.
  3. E. M. Rezler, D. R. Khan, J. Lauer-Fields, M. Cudic, D. Baronas-Lowell, and G. B. Fields, “Targeted drug delivery utilizing protein-like molecular architecture,” Journal of the American Chemical Society, vol. 129, no. 16, pp. 4961–4972, 2007. View at Publisher · View at Google Scholar · View at Scopus
  4. R. Krishna and L. D. Mayer, “The use of liposomal anticancer agents to determine the roles of drug pharmacodistribution and P-glycoprotein (PGP) blockade in overcoming multidrug resistance (MDR),” Anticancer Research, vol. 19, no. 4 B, pp. 2885–2891, 1999. View at Google Scholar · View at Scopus
  5. H. Maeda, J. Wu, T. Sawa, Y. Matsumura, and K. Hori, “Tumor vascular permeability and the EPR effect in macromolecular therapeutics: a review,” Journal of Controlled Release, vol. 65, no. 1-2, pp. 271–284, 2000. View at Publisher · View at Google Scholar · View at Scopus
  6. A. A. Gabizon, “Stealth liposomes and tumor targeting: one step further in the quest for the magic bullet,” Clinical Cancer Research, vol. 7, no. 2, pp. 223–225, 2001. View at Google Scholar · View at Scopus
  7. D. C. Drummond, O. Meyer, K. Hong, D. B. Kirpotin, and D. Papahadjopoulos, “Optimizing liposomes for delivery of chemotherapeutic agents to solid tumors,” Pharmacological Reviews, vol. 51, no. 4, pp. 691–743, 1999. View at Google Scholar · View at Scopus
  8. F. K. Bedu-Addo, P. Tang, Y. Xu, and L. Huang, “Effects of polyethyleneglycol chain length and phospholipid acyl chain composition on the interaction of polyethyleneglycol-phospholipid conjugates with phospholipid: implications in liposomal drug delivery,” Pharmaceutical Research, vol. 13, no. 5, pp. 710–717, 1996. View at Google Scholar · View at Scopus
  9. T. M. Allen, “Liposomes. Opportunities in drug delivery,” Drugs, vol. 54, no. 4, pp. 8–14, 1997. View at Google Scholar · View at Scopus
  10. S. Brown and R. David Khan, “The Treatment of Breast Cancer Using Liposome Technology,” Journal of Drug Delivery, vol. 2012, Article ID 212965, 6 pages, 2012. View at Publisher · View at Google Scholar
  11. J. Gao, W. Zhong, J. He et al., “Tumor-targeted PE38KDEL delivery via PEGylated anti-HER2 immunoliposomes,” International Journal of Pharmaceutics, vol. 374, no. 1-2, pp. 145–152, 2009. View at Publisher · View at Google Scholar · View at Scopus
  12. R. S. Tolhurst, R. S. Thomas, F. J. Kyle et al., “Transient over-expression of estrogen receptor-α in breast cancer cells promotes cell survival and estrogen-independent growth,” Breast Cancer Research and Treatment, vol. 128, no. 2, pp. 357–368, 2011. View at Publisher · View at Google Scholar · View at Scopus
  13. S. R. Paliwal, R. Paliwal, N. Mishra, A. Mehta, and S. P. Vyas, “A novel cancer targeting approach based on estrone anchored stealth liposome for site-specific breast cancer therapy,” Current Cancer Drug Targets, vol. 10, no. 3, pp. 343–353, 2010. View at Publisher · View at Google Scholar · View at Scopus
  14. C. M. Perou, T. Sørile, M. B. Eisen et al., “Molecular portraits of human breast tumours,” Nature, vol. 406, no. 6797, pp. 747–752, 2000. View at Publisher · View at Google Scholar · View at Scopus
  15. T. Sørlie, C. M. Perou, R. Tibshirani et al., “Gene expression patterns of breast carcinomas distinguish tumor subclasses with clinical implications,” Proceedings of the National Academy of Sciences of the United States of America, vol. 98, no. 19, pp. 10869–10874, 2001. View at Publisher · View at Google Scholar · View at Scopus
  16. H. J. Burstein, J. R. Harris, and M. Morrow, “Malignant tumors of the breast,” in De Vita, Hellman and Rosenberg's Cancer, Principles & Practice of Oncology, pp. 1401–1446, Lippincott Williams & Wilkins, 2011. View at Google Scholar
  17. X. Wang, L. Yang, Z. Chen, and D. M. Shin, “Application of nanotechnology in cancer therapy and imaging,” CA Cancer Journal for Clinicians, vol. 58, no. 2, pp. 97–110, 2008. View at Publisher · View at Google Scholar · View at Scopus
  18. D. W. Northfelt, F. J. Martin, P. Working et al., “Doxorubicin encapsulated in liposomes containing surface-bound polyethylene glycol: pharmacokinetics, tumor localization, and safety in patients with AIDS-related Kaposi's sarcoma,” Journal of Clinical Pharmacology, vol. 36, no. 1, pp. 55–63, 1996. View at Google Scholar · View at Scopus
  19. Z. Symon, A. Peyser, D. Tzemach et al., “Selective delivery of doxorubicin to patients with breast carcinoma metastases by stealth liposomes,” Cancer, vol. 86, pp. 72–78, 1999. View at Google Scholar
  20. T. A. Elbayoumi and V. P. Torchilin, “Tumor-specific antibody-mediated targeted delivery of Doxil reduces the manifestation of auricular erythema side effect in mice,” International Journal of Pharmaceutics, vol. 357, no. 1-2, pp. 272–279, 2008. View at Publisher · View at Google Scholar · View at Scopus
  21. “Preclinical development: tissue distribution of doxorubicin (DOX) and TLC D-99 and conventional doxorubicin,” Data from the Registration dossier.
  22. D. D. Von Hoff, M. W. Layard, and P. Basa, “Risk factors for doxorubicin-induced congestive heart failure,” Annals of Internal Medicine, vol. 91, no. 5, pp. 710–717, 1979. View at Google Scholar · View at Scopus
  23. L. J. Steinherz, P. G. Steinherz, C. T. C. Tan, G. Heller, and M. L. Murphy, “Cardiac toxicity 4 to 20 years after completing anthracycline therapy,” Journal of the American Medical Association, vol. 266, no. 12, pp. 1672–1677, 1991. View at Publisher · View at Google Scholar · View at Scopus
  24. N. G. Fisher and A. J. Marshall, “Anthracycline-induced cardiomyopathy,” Postgraduate Medical Journal, vol. 75, no. 883, pp. 265–268, 1999. View at Google Scholar · View at Scopus
  25. A. P. Launchbury and N. Habboubi, “Epirubicin and doxorubicin: a comparison of their characteristics, therapeutic activity and toxicity,” Cancer Treatment Reviews, vol. 19, no. 3, pp. 197–228, 1993. View at Publisher · View at Google Scholar · View at Scopus
  26. M. E. Billingham, J. W. Mason, M. R. Bristow, and J. R. Daniels, “Anthracycline cardiomyopathy monitored by morphologic changes,” Cancer Treatment Reports, vol. 62, no. 6, pp. 865–872, 1978. View at Google Scholar · View at Scopus
  27. R. G. Schwartz, W. B. McKenzie, J. Alexander et al., “Congestive heart failure and left ventricular dysfunction complicating doxorubicin therapy. Seven-year experience using serial radionuclide angiocardiography,” The American Journal of Medicine, vol. 82, no. 6, pp. 1109–1118, 1987. View at Google Scholar · View at Scopus
  28. M. F. Stoddard, J. Seeger, N. E. Liddell, T. J. Hadley, D. M. Sullivan, and J. Kupersmith, “Prolongation of isovolumetric relaxation time as assessed by Doppler echocardiography predicts doxorubicin-induced systolic dysfunction in humans,” Journal of the American College of Cardiology, vol. 20, no. 1, pp. 62–69, 1992. View at Google Scholar · View at Scopus
  29. W. I. Ganz, K. S. Sridhar, and T. J. Forness, “Detection of early anthracycline cardiotoxicity by monitoring the peak filling rate,” The American Journal of Clinical Oncology, vol. 16, no. 2, pp. 109–112, 1993. View at Google Scholar · View at Scopus
  30. S. M. Swain, F. S. Whaley, and M. S. Ewer, “Congestive heart failure in patients treated with doxorubicin: a retrospective analysis of three trials,” Cancer, vol. 97, no. 11, pp. 2869–2879, 2003. View at Publisher · View at Google Scholar · View at Scopus
  31. C. L. Shapiro, P. H. Hardenbergh, R. Gelman et al., “Cardiac effects of adjuvant doxorubicin and radiation therapy in breast cancer patients,” Journal of Clinical Oncology, vol. 16, no. 11, pp. 3493–3501, 1998. View at Google Scholar · View at Scopus
  32. C. L. Shapiro and A. Recht, “Side effects of adjuvant treatment of breast cancer,” The New England Journal of Medicine, vol. 344, no. 26, pp. 1997–2008, 2001. View at Publisher · View at Google Scholar · View at Scopus
  33. M. E. O'Brien, N. Wigler, M. Inbar et al., “Reduced cardiotoxicity and comparable efficacy in a phase III trial of pegylated liposomal doxorubicin HCI, (CAELYX/Doxil) versus conventional doxorubicin for first-line treatment of metastasic breast cancer,” Annals of Oncology, vol. 15, no. 3, pp. 440–449, 2004. View at Google Scholar
  34. L. Harris, G. Batist, R. Belt et al., “Liposome-encapsulated doxorubicin compared with conventional doxorubicin in a randomized multicenter trial as first-line therapy of metastatic breast carcinoma,” Cancer, vol. 94, no. 1, pp. 25–36, 2002. View at Publisher · View at Google Scholar · View at Scopus
  35. G. Batist, G. Ramakrishnan, C. S. Rao et al., “Reduced cardiotoxicity and preserved antitumor efficacy of liposome-encapsulated doxorubicin and cyclophosphamide compared with conventional doxorubicin and cyclophosphamide in a randomized, multicenter trial of metastatic breast cancer,” Journal of Clinical Oncology, vol. 19, no. 5, pp. 1444–1454, 2001. View at Google Scholar · View at Scopus
  36. S. Chan, N. Davidson, E. Juozaityte et al., “Phase III trial of liposomal doxorubicin and ciclophosphamide compared with epirrubicin and ciclophosphamide as first-line therapy for metastasic breast cancer,” Annals of Oncology, vol. 15, pp. 1527–1534, 2004. View at Google Scholar
  37. J. A. Sparano, A. N. Makhson, V. F. Semiglazov et al., “Pegylated liposomal doxorubicin plus docetaxel significantly improves time to progression without additive cardiotoxicity compared with docetaxel monotherapy in patients with advanced breast cancer previously treated with neoadjuvant-adjuvant anthracycline therapy: results from a randomized phase III study,” Journal of Clinical Oncology, vol. 27, no. 27, pp. 4522–4529, 2009. View at Publisher · View at Google Scholar · View at Scopus
  38. L. Gianni, E. Munzone, G. Capri et al., “Paclitaxel by 3-hour infusion in combination with bolus doxorubicin in women with untreated metastatic breast cancer: high antitumor efficacy and cardiac effects in a dose-finding and sequence-finding study,” Journal of Clinical Oncology, vol. 13, no. 11, pp. 2688–2699, 1995. View at Google Scholar · View at Scopus
  39. L. Gianni, L. Viganò, A. Locatelli et al., “Human pharmacokinetic characterization and in vitro study of the interaction between doxorubicin and paclitaxel in patients with breast cancer,” Journal of Clinical Oncology, vol. 15, no. 5, pp. 1906–1915, 1997. View at Google Scholar · View at Scopus
  40. D. J. Slamon, B. Leyland-Jones, S. Shak et al., “Use of chemotherapy plus a monoclonal antibody against her2 for metastatic breast cancer that overexpresses HER2,” The New England Journal of Medicine, vol. 344, no. 11, pp. 783–792, 2001. View at Publisher · View at Google Scholar · View at Scopus
  41. M. Untch, H. Eidtmann, A. Du Bois et al., “Cardiac safety of trastuzumab in combination with epirubicin and cyclophosphamide in women with metastatic breast cancer: results of a phase I trial,” European Journal of Cancer, vol. 40, no. 7, pp. 988–997, 2004. View at Publisher · View at Google Scholar · View at Scopus
  42. A. N. Gordon, J. T. Fleagle, D. Guthrie, D. E. Parkin, M. E. Gore, and A. J. Lacave, “Recurrent epithelial ovarian carcinoma: a randomized phase III study of pegylated liposomal doxorubicin versus topotecan,” Journal of Clinical Oncology, vol. 19, no. 14, pp. 3312–3322, 2001. View at Google Scholar · View at Scopus
  43. M. S. Rosati, C. Raimondi, G. Baciarello et al., “Weekly combination of non-pegylated liposomal doxorubicin and taxane in first-line breast cancer: wALT trial (phase I-II),” Annals of Oncology, vol. 22, no. 2, pp. 315–320, 2011. View at Publisher · View at Google Scholar · View at Scopus
  44. P. Schmid, J. Krocker, R. Kreienberg et al., “Non-pegylated liposomal doxorubicin and docetaxel in metastatic breast cancer: final results of a phase II trial,” Cancer Chemotherapy and Pharmacology, vol. 64, no. 2, pp. 401–406, 2009. View at Publisher · View at Google Scholar · View at Scopus
  45. E. Curtit, P. Nouyrigat, N. Dohollou, E. Levy et al., “Myotax: a phase II trial of docetaxel plus non-pegylated liposomal doxorubicin as first-line therapy of metastatic breast cancer previously treated with adjuvant,” European Journal of Cancer, vol. 47, no. 16, pp. 2396–2402.
  46. C. Rochlitz, T. Ruhstaller, S. Lerch et al., “Combination of bevacizumab and 2-weekly pegylated liposomal doxorubicin as first-line therapy for locally recurrent or metastatic breast cancer. A multicenter, single-arm phase II trial (SAKK 24/06),” Annals of Oncology, vol. 22, no. 1, pp. 80–85, 2011. View at Publisher · View at Google Scholar · View at Scopus
  47. G. Batist, L. Harris, N. Azarnia, L. W. Lee, and P. Daza-Ramirez, “Improved anti-tumor response rate with decreased cardiotoxicity of non-pegylated liposomal doxorubicin compared with conventional doxorubicin in first-line treatment of metastatic breast cancer in patients who had received prior adjuvant doxorubicin: results of a retrospective analysis,” Anti-Cancer Drugs, vol. 17, no. 5, pp. 587–595, 2006. View at Google Scholar · View at Scopus
  48. E. C. Van Dalen, E. M. C. Michiels, H. N. Caron, and L. C. M. Kremer, “Different anthracycline derivatives for reducing cardiotoxicity in cancer patients,” Cochrane Database of Systematic Reviews, no. 3, 2010. View at Google Scholar · View at Scopus
  49. A. M. Keller, R. G. Mennel, V. A. Georgoulias et al., “Randomized phase III trial of pegylated liposomal doxorubicin versus vinorelbine or mitomycin C plus vinblastine in women with taxane-refractory advanced breast cancer,” Journal of Clinical Oncology, vol. 22, no. 19, pp. 3893–3901, 2004. View at Publisher · View at Google Scholar · View at Scopus
  50. M. Fiegl, B. Mlineritsch, M. Hubalek, R. Bartsch, U. Pluschnig, and G. G. Steger, “Single-agent pegylated liposomal doxorubicin (PLD) in the treatment of metastatic breast cancer: results of an Austrian observational trial,” BMC Cancer, vol. 11, Article ID 373, 2011. View at Publisher · View at Google Scholar
  51. E. Alba, M. Ruiz-Borrego, M. Margelí et al., “Maintenance treatment with Pegylated liposomal doxorubicin versus observation following induction chemotherapy for metastatic breast cancer: GEICAM 2001-01 study,” Breast Cancer Research and Treatment, vol. 122, no. 1, pp. 169–176, 2010. View at Publisher · View at Google Scholar · View at Scopus
  52. M. D. Pegram, T. Pienkowski, D. W. Northfelt et al., “Results of two open-label, multicenter phase II studies of docetaxel, platinum salts, and trastuzumab in HER2-positive advanced breast cancer,” Journal of the National Cancer Institute, vol. 96, no. 10, pp. 759–769, 2004. View at Google Scholar · View at Scopus
  53. D. Slamon, W. Eiermann, N. Robert et al., “Adjuvant trastuzumab in her-2 positive breast cancer,” The New England Journal of Medicine, vol. 365, no. 14, pp. 1273–1283, 2011. View at Google Scholar
  54. M. Untch, M. Muscholl, S. Tjulandin et al., “First-line trastuzumab plus epirubicin and cyclophosphamide therapy in patients with human epidermal growth factor receptor 2-positive metastatic breast cancer: cardiac safety and efficacy data from the herceptin, cyclophosphamide, and epirubicin (HERCULES) trial,” Journal of Clinical Oncology, vol. 28, no. 9, pp. 1473–1480, 2010. View at Publisher · View at Google Scholar · View at Scopus
  55. M. Theodoulou, S. M. Campos, L. Welles et al., “TLC D99 (D, Myocet) and Herceptin (H) is safe in advanced breast cancer (ABC): final cardiac safety and efficacy analysis,” Proceedings of the American Society of Clinical Oncology, vol. 21, Abstract 216, 2002. View at Google Scholar · View at Scopus
  56. J. Cortes, S. DiCosimo, M. A. Climent et al., “Nonpegylated liposomal doxorubicin (TLC-D99), Paclitaxel, and Trastuzumab in HER-2-overexpressing breast cancer: a multicenter phase l/ll study,” Clinical Cancer Research, vol. 15, no. 1, pp. 307–314, 2009. View at Publisher · View at Google Scholar · View at Scopus
  57. M. Venturini, C. Bighin, F. Puglisi et al., “A multicentre phase II study of non-pegylated liposomal doxorubicin in combination with trastuzumab and docetaxel as first-line therapy in metastatic breast cancer,” Breast, vol. 19, no. 5, pp. 333–338, 2010. View at Publisher · View at Google Scholar · View at Scopus
  58. D. Amadori, C. Milandri, G. Comella et al., “A phase I/II trial of nonpegylated liposomal doxorubicin, docetaxel, and trastuzumab as first-line treatment in HER-2-positive locally advanced or metastatic breast cancer,” European Journal of Cancer, vol. 47, no. 14, pp. 2091–2098, 2011. View at Google Scholar
  59. S. Chia, M. Clemons, L. A. Martin et al., “Pegylated liposomal doxorubicin and trastuzumab in HER-2 overexpressing metastatic breast cancer: a multicenter phase II trial,” Journal of Clinical Oncology, vol. 24, no. 18, pp. 2773–2778, 2006. View at Publisher · View at Google Scholar · View at Scopus
  60. E. Andreopoulou, D. Gaiotti, E. Kim et al., “Feasibility and cardiac safety of pegylated liposomal doxorubicin plus trastuzumab in heavily pretreated patients with recurrent HER2-overexpressing metastatic breast cancer,” Clinical Breast Cancer, vol. 7, no. 9, pp. 690–696, 2007. View at Publisher · View at Google Scholar · View at Scopus
  61. E. Stickeler, M. Klar, D. Watermann et al., “Pegylated liposomal doxorubicin and trastuzumab as 1st and 2nd line therapy in her2/neu positive metastatic breast cancer: a multicenter phase II trial,” Breast Cancer Research and Treatment, vol. 117, no. 3, pp. 591–598, 2009. View at Publisher · View at Google Scholar · View at Scopus
  62. C. Christodoulou, I. Kostopoulos, H. P. Kalofonos et al., “Trastuzumab combined with pegylated liposomal doxorubicin in patients with metastatic breast cancer: phase II study of the hellenic cooperative oncology group (HeCOG) with biomarker evaluation,” Oncology, vol. 76, no. 4, pp. 275–285, 2009. View at Publisher · View at Google Scholar · View at Scopus
  63. A. C. Wolff, M. Wang, H. Li et al., “Phase II trial of pegylated liposomal doxorubicin plus docetaxel with and without trastuzumab in metastatic breast cancer: eastern cooperative oncology group trial E3198,” Breast Cancer Research and Treatment, vol. 121, no. 1, pp. 111–120, 2010. View at Publisher · View at Google Scholar · View at Scopus
  64. M. Martín, M. Muñoz, J. M. Baena-Cañada et al., “Pegylated liposomal doxorubicin in combination with cyclophosphamide and trastuzumab in HER2-positive metastatic breast cancer patients: efficacy and cardiac safety from the GEICAM/2004-05 study,” Annals of Oncology, vol. 22, no. 12, Article ID mdr024, pp. 2591–2596, 2011. View at Publisher · View at Google Scholar
  65. K. Possinger, J. Krocker, J. Fritz et al., “Primary chemotherapy for locally advanced breast cancer (LABC) with gemcitabine (G) as prolonged infusion, liposomal doxorubicin (M) and Docetaxel (T): results of a phase I trial,” Proceedings of the American Society of Clinical Oncology, vol. 21, abstract 1971, 2002. View at Google Scholar
  66. H. Gogas, C. Papadimitriou, H. P. Kalofonos et al., “Neoadjuvant chemotherapy with a combination of pegylated liposomal doxorubicin (Caelyx) and paclitaxel in locally advanced breast cancer: a phase II study by the Hellenic cooperative oncology group,” Annals of Oncology, vol. 13, no. 11, pp. 1737–1742, 2002. View at Publisher · View at Google Scholar · View at Scopus
  67. A. Gennari, M. P. Sormani, P. Pronzato et al., “HER2 status and efficacy of adjuvant anthracyclines in early breast cancer: a pooled analysis of randomized trials,” Journal of the National Cancer Institute, vol. 100, no. 1, pp. 14–20, 2008. View at Publisher · View at Google Scholar · View at Scopus
  68. A. Antón, A. Ruiz, M. A. Seguí et al., “Phase I clinical trial of liposomal-encapsulated doxorubicin citrate and docetaxel, associated with trastuzumab, as neo-adjuvant treatment in stages II and IIIA, HER2-overexpressing breast cancer patients. GEICAM 2003-03 study,” Annals of Oncology, vol. 20, no. 3, pp. 454–459, 2009. View at Publisher · View at Google Scholar · View at Scopus
  69. A. Antón, A. Ruiz, A. Plazaola et al., “Phase II clinical trial of liposomal-encapsulated doxorubicin citrate and docetaxel, associated with trastuzumab, as neoadjuvant treatment in stages II and IIIA HER2-overexpressing breast cancer patients. GEICAM 2003-03 study,” Annals of Oncology, vol. 22, no. 1, pp. 74–79, 2011. View at Publisher · View at Google Scholar · View at Scopus
  70. D. Rayson, T. M. Suter, C. Jackisch et al., “Cardiac safety of adjuvant pegylated liposomal doxorubicin with concurrent trastuzumab: a randomized phase II trial,” Annals of Oncology, vol. 23, no. 7, Article ID mdr519, pp. 1780–1788, 2012. View at Publisher · View at Google Scholar