Accelerated blood clearance (ABC) phenomenon upon repeated injection of PEGylated liposomes

International Journal of Pharmaceutics

Volumn 354, Issue 1-2, 2008, Pages 56-62

  Ishida, Tatsuhiro ^a   Kiwada, Hiroshi ^a  

^a Institute of Health Biosciences   (Japan)

Author keywords

Accelerated blood clearance (ABC) phenomenon; Complement activation; IgM; Liposomes; Polyethylene glycol (PEG); Repeated injection

Indexed keywords

DOXORUBICIN; IMMUNOGLOBULIN M; LIPOSOME; PEGYLATED IMMUNOGLOBULIN M; PEGYLATED LIPOSOME DERIVATIVE; UNCLASSIFIED DRUG;

DRUG FORMULATION; ENCAPSULATION; IMMUNOGENICITY; PHYSICAL CHEMISTRY; PLASMA CLEARANCE; PRIORITY JOURNAL; SHORT SURVEY;

ANIMALS; COMPLEMENT ACTIVATION; DRUG ADMINISTRATION SCHEDULE; DRUG CARRIERS; IMMUNOGLOBULIN M; INJECTIONS, INTRAVENOUS; LIPOSOMES; POLYETHYLENE GLYCOLS;

EID: 40849138014     PISSN: 03785173     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ijpharm.2007.11.005     Document Type: Short Survey

References (59)

1. Allen T.M., Austin G.A., Chonn A., Lin L., and Lee K.C. Uptake of liposomes by cultured mouse bone marrow macrophages: influence of liposome composition and size. Biochim. Biophys. Acta 1061 (1991) 56-64
2. Allen T.M., Hansen C., Martin F., Redemann C., and Yau-Young A. Liposomes containing synthetic lipid derivatives of poly(ethylene glycol) show prolonged circulation half-lives in vivo. Biochim. Biophys. Acta 1066 (1991) 29-36
3. Blume G., and Cevc G. Liposomes for the sustained drug release in vivo. Biochim. Biophys. Acta 1029 (1990) 91-97
4. Bourgeois H., Ferru A., Lortholary A., Delozier T., Boisdron-Celle M., Abadie-Lacourtoisie S., Joly F., Chieze S., Chabrun V., Gamelin E., and Tourani J.M. Phase I-II study of pegylated liposomal doxorubicin combined with weekly paclitaxel as first-line treatment in patients with metastatic breast cancer. Am. J. Clin. Oncol. 29 (2006) 267-275
5. Caraglia M., Addeo R., Costanzo R., Montella L., Faiola V., Marra M., Abbruzzese A., Palmieri G., Budillon A., Grillone F., Venuta S., Tagliaferri P., and Del Prete S. Phase II study of temozolomide plus pegylated liposomal doxorubicin in the treatment of brain metastases from solid tumours. Cancer Chemother. Pharmacol. 57 (2006) 34-39
6. Carignano M.A., and Szleifer I.I. Prevention of protein adsorption by flexible and rigid chain molecules. Colloids Surf. B Biointerfaces 18 (2000) 169-182
7. Chidiac T., Budd G.T., Pelley R., Sandstrom K., McLain D., Elson P., Crownover R., Marks K., Muschler G., Joyce M., Zehr R., and Bukowski R. Phase II trial of liposomal doxorubicin (Doxil) in advanced soft tissue sarcomas. Invest. New Drugs 18 (2000) 253-259
8. Chonn A., Semple S.C., and Cullis P.R. Association of blood proteins with large unilamellar liposomes in vivo. Relation to circulation lifetimes. J. Biol. Chem. 267 (1992) 18759-18765
9. Coleman R.E., Biganzoli L., Canney P., Dirix L., Mauriac L., Chollet P., Batter V., Ngalula-Kabanga E., Dittrich C., and Piccart M. A randomised phase II study of two different schedules of pegylated liposomal doxorubicin in metastatic breast cancer (EORTC-10993). Eur. J. Cancer 42 (2006) 882-887
10. Dams E.T., Laverman P., Oyen W.J., Storm G., Scherphof G.L., van Der Meer J.W., Corstens F.H., and Boerman O.C. Accelerated blood clearance and altered biodistribution of repeated injections of sterically stabilized liposomes. J. Pharmacol. Exp. Ther. 292 (2000) 1071-1079
11. de Gennes P.G. Conformation of polymers attached to an interface. Macromolecules 13 (1980) 1069-1075
12. Elbert D.L., and Hubbell J.A. Surface treatments of polymers for biocompatibility. Ann. Rev. Mater. Sci. 26 (1996) 365-394
13. Escobar P.F., Markman M., Zanotti K., Webster K., and Belinson J. Phase 2 trial of pegylated liposomal doxorubicin in advanced endometrial cancer. J. Cancer Res. Clin. Oncol. 129 (2003) 651-654
14. Gabizon A.A., Barenholz Y., and Bialer M. Prolongation of the circulation time of doxorubicin encapsulated in liposomes containing a polyethylene glycol-derivatized phospholipid: pharmacokinetic studies in rodents and dogs. Pharm. Res. 10 (1993) 703-708
15. Gnad-Vogt S.U., Hofheinz R.D., Saussele S., Kreil S., Willer A., Willeke F., Pilz L., Hehlmann R., and Hochhaus A. Pegylated liposomal doxorubicin and mitomycin C in combination with infusional 5-fluorouracil and sodium folinic acid in the treatment of advanced gastric cancer: results of a phase II trial. Anticancer Drugs 16 (2005) 435-440
16. Goins B., Phillips W.T., and Klipper R. Repeat injection studies of technetium-99m-labeled PEG-liposomes in the same animal. J. Liposome Res. 8 (1998) 265-281
17. Grunaug M., Bogner J.R., Loch O., and Goebel F.D. Liposomal doxorubicin in pulmonary Kaposi's sarcoma: improved survival as compared to patients without liposomal doxorubicin. Eur. J. Med. Res. 3 (1998) 13-19
18. Halm U., Etzrodt G., Schiefke I., Schmidt F., Witzigmann H., Mossner J., and Berr F. A phase II study of pegylated liposomal doxorubicin for treatment of advanced hepatocellular carcinoma. Ann. Oncol. 11 (2000) 113-114
19. Hubert A., Lyass O., Pode D., and Gabizon A. Doxil (Caelyx): an exploratory study with pharmacokinetics in patients with hormone-refractory prostate cancer. Anticancer Drugs 11 (2000) 123-127
20. Ishida T., Atobe K., Wang X., and Kiwada H. Accelerated blood clearance of PEGylated liposomes upon repeated injections: effect of doxorubicin-encapsulation and high-dose first injection. J. Control Release 115 (2006) 251-258
21. Ishida T., Harada M., Wang X.Y., Ichihara M., Irimura K., and Kiwada H. Accelerated blood clearance of PEGylated liposomes following preceding liposome injection: effects of lipid dose and PEG surface-density and chain length of the first-dose liposomes. J. Control Release 105 (2005) 305-317
22. Ishida T., Ichihara M., Wang X., and Kiwada H. Spleen plays an important role in the induction of accelerated blood clearance of PEGylated liposomes. J. Control Release 115 (2006) 243-250
23. Ishida T., Ichihara M., Wang X., Yamamoto K., Kimura J., Majima E., and Kiwada H. Injection of PEGylated liposomes in rats elicits PEG-specific IgM, which is responsible for rapid elimination of a second dose of PEGylated liposomes. J. Control Release 112 (2006) 15-25
24. Ishida T., Ichikawa T., Ichihara M., Sadzuka Y., and Kiwada H. Effect of the physicochemical properties of initially injected liposomes on the clearance of subsequently injected PEGylated liposomes in mice. J. Control Release 95 (2004) 403-412
25. Ishida T., Maeda R., Ichihara M., Irimura K., and Kiwada H. Accelerated clearance of PEGylated liposomes in rats after repeated injections. J. Control Release 88 (2003) 35-42
26. Ishida T., Maeda R., Ichihara M., Mukai Y., Motoki Y., Manabe Y., Irimura K., and Kiwada H. The accelerated clearance on repeated injection of PEGylated liposomes in rats: laboratory and histopathological study. Cell Mol. Biol. Lett. 7 (2002) 286
27. Ishida T., Masuda K., Ichikawa T., Ichihara M., Irimura K., and Kiwada H. Accelerated clearance of a second injection of PEGylated liposomes in mice. Int. J. Pharm. 255 (2003) 167-174
28. Ishida T., Wang X.Y., Shimizu T., Nawata K., and Kiwada H. PEGylated liposomes elicit an anti-PEG IgM response in a T cell-independent manner. J. Control Release 122 (2007) 349-355
29. Katsaros D., Oletti M.V., Rigault de la Longrais I.A., Ferrero A., Celano A., Fracchioli S., Donadio M., Passera R., Cattel L., and Bumma C. Clinical and pharmacokinetic phase II study of pegylated liposomal doxorubicin and vinorelbine in heavily pretreated recurrent ovarian carcinoma. Ann. Oncol. 16 (2005) 300-306
30. Klibanov A.L., Maruyama K., Torchilin V.P., and Huang L. Amphipathic polyethyleneglycols effectively prolong the circulation time of liposomes. FEBS Lett. 268 (1990) 235-237
31. Koukourakis M.I., Koukouraki S., Giatromanolaki A., Archimandritis S.C., Skarlatos J., Beroukas K., Bizakis J.G., Retalis G., Karkavitsas N., and Helidonis E.S. Liposomal doxorubicin and conventionally fractionated radiotherapy in the treatment of locally advanced non-small-cell lung cancer and head and neck cancer. J. Clin. Oncol. 17 (1999) 3512-3521
32. Krown S.E., Northfelt D.W., Osoba D., and Stewart J.S. Use of liposomal anthracyclines in Kaposi's sarcoma. Semin. Oncol. 31 (2004) 36-52
33. Lasic D.D., Martin F.J., Gabizon A., Huang S.K., and Papahadjopoulos D. Sterically stabilized liposomes: a hypothesis on the molecular origin of the extended circulation times. Biochim. Biophys. Acta 1070 (1991) 187-192
34. Laverman P., Carstens M.G., Boerman O.C., Dams E.T., Oyen W.J., van Rooijen N., Corstens F.H., and Storm G. Factors affecting the accelerated blood clearance of polyethylene glycol-liposomes upon repeated injection. J. Pharmacol. Exp. Ther. 298 (2001) 607-612
35. Lee J.H., Lee H.B., and Andrade J.D. Blood compatibility of polyethylene oxide surface. Prog. Polymer Sci. 20 (1995) 1043-1049
36. Lyass O., Uziely B., Ben-Yosef R., Tzemach D., Heshing N.I., Lotem M., Brufman G., and Gabizon A. Correlation of toxicity with pharmacokinetics of pegylated liposomal doxorubicin (Doxil) in metastatic breast carcinoma. Cancer 89 (2000) 1037-1047
37. Markman M., Kennedy A., Webster K., Peterson G., Kulp B., and Belinson J. Phase 2 trial of liposomal doxorubicin (40 mg/m(2)) in platinum/paclitaxel-refractory ovarian and fallopian tube cancers and primary carcinoma of the peritoneum. Gynecol. Oncol. 78 (2000) 369-372
38. Martin F., Oliver A.M., and Kearney J.F. Marginal zone and B1 B cells unite in the early response against T-independent blood-borne particulate antigens. Immunity 14 (2001) 617-629
39. Maruyama K., Yuda T., Okamoto A., Kojima S., Suginaka A., and Iwatsuru M. Prolonged circulation time in vivo of large unilamellar liposomes composed of distearoyl phosphatidylcholine and cholesterol containing amphipathic poly(ethylene glycol). Biochim. Biophys. Acta 1128 (1992) 44-49
40. Mirchandani D., Hochster H., Hamilton A., Liebes L., Yee H., Curtin J.P., Lee S., Sorich J., Dellenbaugh C., and Muggia F.M. Phase I study of combined pegylated liposomal doxorubicin with protracted daily topotecan for ovarian cancer. Clin. Cancer Res. 11 (2005) 5912-5919
41. Muggia F.M., Hainsworth J.D., Jeffers S., Miller P., Groshen S., Tan M., Roman L., Uziely B., Muderspach L., Garcia A., Burnett A., Greco F.A., Morrow C.P., Paradiso L.J., and Liang L.J. Phase II study of liposomal doxorubicin in refractory ovarian cancer: antitumor activity and toxicity modification by liposomal encapsulation. J. Clin. Oncol. 15 (1997) 987-993
42. Needham D., McIntosh T.J., and Lasic D.D. Repulsive interactions and mechanical stability of polymer-grafted lipid membranes. Biochim. Biophys. Acta 1108 (1992) 40-48
43. Needham D., Stoicheva N., and Zhelev D.V. Exchange of monooleoylphosphatidylcholine as monomer and micelle with membranes containing poly(ethylene glycol)-lipid. Biophys. J. 73 (1997) 2615-2629
44. Nikolova A.N., and Jones M.N. Effect of grafted PEG-2000 on the size and permeability of vesicles. Biochim. Biophys. Acta 1304 (1996) 120-128
45. Orditura M., Quaglia F., Morgillo F., Martinelli E., Lieto E., De Rosa G., Comunale D., Diadema M.R., Ciardiello F., Catalano G., and De Vita F. Pegylated liposomal doxorubicin: pharmacologic and clinical evidence of potent antitumor activity with reduced anthracycline-induced cardiotoxicity (review). Oncol. Rep. 12 (2004) 549-556
46. Oussoren C., and Storm G. Effect of repeated intravenous administration on circulation kinetics of poly(ethyleneglycol)-liposomes in rats. J. Liposome Res. 9 (1998) 349-355
47. Overmoyer B., Silverman P., Holder L.W., Tripathy D., and Henderson I.C. Pegylated liposomal doxorubicin and cyclophosphamide as first-line therapy for patients with metastatic or recurrent breast cancer. Clin. Breast Cancer 6 (2005) 150-157
48. Papahadjopoulos D., Allen T.M., Gabizon A., Mayhew E., Matthay K., Huang S.K., Lee K.D., Woodle M.C., Lasic D.D., Redemann C., et al. Sterically stabilized liposomes: improvements in pharmacokinetics and antitumor therapeutic efficacy. Proc. Natl. Acad. Sci. U.S.A. 88 (1991) 11460-11464
49. Poh S.B., Bai L.Y., and Chen P.M. Pegylated liposomal doxorubicin-based combination chemotherapy as salvage treatment in patients with advanced hepatocellular carcinoma. Am. J. Clin. Oncol. 28 (2005) 540-546
50. Satulovsky J., Carignano M.A., and Szleifer I. Kinetic and thermodynamic control of protein adsorption. Proc. Natl. Acad. Sci. U.S.A. 97 (2000) 9037-9041
51. Senior J., Delgado C., Fisher D., Tilcock C., and Gregoriadis G. Influence of surface hydrophilicity of liposomes on their interaction with plasma protein and clearance from the circulation: studies with poly(ethylene glycol)-coated vesicles. Biochim. Biophys. Acta 1062 (1991) 77-82
52. Tardi P.G., Swartz E.N., Harasym T.O., Cullis P.R., and Bally M.B. An immune response to ovalbumin covalently coupled to liposomes is prevented when the liposomes used contain doxorubicin. J. Immunol. Methods 210 (1997) 137-148
53. Torchilin V.P., Omelyanenko V.G., Papisov M.I., Bogdanov Jr. A.A., Trubetskoy V.S., Herron J.N., and Gentry C.A. Poly(ethylene glycol) on the liposome surface: on the mechanism of polymer-coated liposome longevity. Biochim. Biophys. Acta 1195 (1994) 11-20
54. Verhaar-Langereis M., Karakus A., van Eijkeren M., Voest E., and Witteveen E. Phase II study of the combination of pegylated liposomal doxorubicin and topotecan in platinum-resistant ovarian cancer. Int. J. Gynecol. Cancer 16 (2006) 65-70
55. Wang X.Y., Ishida T., Ichihara M., and Kiwada H. Influence of the physicochemical properties of liposomes on the accelerated blood clearance phenomenon in rats. J. Control Release 104 (2005) 91-102
56. Wang X.Y., Ishida T., and Kiwada H. Anti-PEG IgM elicited by injection of liposomes is involved in the enhanced blood clearance of a subsequent dose of PEGylated liposomes. J. Control Release 119 (2007) 236-244
57. Woodle M.C. Controlling liposome blood clearance by surface-grafted polymers. Adv. Drug Deliv. Rev. 32 (1998) 139-152
58. Woodle M.C., and Lasic D.D. Sterically stabilized liposomes. Biochim. Biophys. Acta 1113 (1992) 171-199
59. Zandvoort A., and Timens W. The dual function of the splenic marginal zone: essential for initiation of anti-TI-2 responses but also vital in the general first-line defense against blood-borne antigens. Clin. Exp. Immunol. 130 (2002) 4-11