Issues in long-term protein delivery using biodegradable microparticles

Journal of Controlled Release

Volumn 146, Issue 2, 2010, Pages 241-260

  Ye, Mingli ^a   Kim, Sungwon ^a   Park, Kinam ^a  

^a PURDUE UNIVERSITY   (United States)

Author keywords

Burst release; Emulsion method; Encapsulation efficiency; Loading efficiency; Microparticles; PLGA; Protein drug; Release profile

Indexed keywords

BIOACTIVITY; BIODEGRADABLE POLYMERS; CONTROLLED DRUG DELIVERY; DRUG PRODUCTS; EFFICIENCY; EMULSIFICATION; ENZYMES; TARGETED DRUG DELIVERY;

BURST RELEASE; EMULSION METHOD; ENCAPSULATION EFFICIENCY; LOADING EFFICIENCY; MICRO-PARTICLES; PLGA; PROTEIN DRUGS; RELEASE PROFILES;

LOADING;

ALPHA2B INTERFERON; AUTOLOGOUS FIXED TUMOR VACCINE; BOVINE SERUM ALBUMIN; BRAIN DERIVED NEUROTROPHIC FACTOR; CHORIONIC GONADOTROPIN; CHYMOTRYPSIN A; ERYTHROPOIETIN; EXENDIN 4; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR; GOSERELIN; GROWTH FACTOR; HUMAN GROWTH HORMONE; INSULIN; LEUPRORELIN; LYSOZYME; MALARIA VACCINE; MICROSPHERE; OCTREOTIDE; OIL; OVALBUMIN; PEPTIDE VACCINE; POLYGLACTIN; RECOMBINANT ERYTHROPOIETIN; TRIPTORELIN; TUMOR VACCINE; UNCLASSIFIED DRUG; UNINDEXED DRUG; V3 PEPTIDE VACCINE; VAPREOTIDE; VASCULOTROPIN; WATER;

ACROMEGALY; BIOTECHNOLOGY; BREAST CANCER; CLINICAL TRIAL; DRUG DELIVERY SYSTEM; DRUG RELEASE; ELECTROSPRAY; EMULSION; ENDOMETRIOSIS; FREEZE DRYING; GLIOBLASTOMA; GROWTH HORMONE DEFICIENCY; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; LIVER CELL CARCINOMA; MICROENCAPSULATION; MICROFLUIDIC ANALYSIS; NEBULIZATION; NEUROENDOCRINE TUMOR; PARTICLE SIZE; PRIORITY JOURNAL; PROSTATE CANCER; PROTEIN DELIVERY SYSTEM; PROTEIN PROCESSING; PROTEIN SECRETION; REVIEW; SPRAY DRYING;

EID: 77955418929     PISSN: 01683659     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jconrel.2010.05.011     Document Type: Review

References (182)

1. Cohen S., Yoshioka T., Lucarelli M., Hwang L.H., Langer R. Controlled delivery systems for proteins based on poly(lactic/glycolic acid) microspheres. Pharm. Res. 1991, 8(6):713-720.
2. Johnson O.L., Tracy M.A. Encyclopedia of Controlled Drug Delivery 1999, Vol. 2:816-832. John Wiley and Sons, New Jersey. E. Mathiowitz (Ed.).
3. Leach W.T., Simpson D.T., Val T.N., Anuta E.C., Yu Z., Williams R.O., Johnston K.P. Uniform encapsulation of stable protein nanoparticles produced by spray freezing for the reduction of burst release. J. Pharm. Sci. 2005, 94(1):56-69.
4. Morlock M.K., H., Winter G., Kissel T. Microencapsulation of rh-erythropoietin, using biodegradable poly(d,l-lactide-co-glycolide): protein stability and the effects of stabilizing excipients. Eur. J. Pharm. Biopharm. 1997, 43:29-36.
5. Takada S., Yamagata Y., Misaki M., Taira K., Kurokawa T. Sustained release of human growth hormone from microcapsules prepared by a solvent evaporation technique. J. Control. Release 2003, 88(2):229-242.
6. Pean J.M., Boury F., Venier-Julienne M.C., Menei P., Proust J.E., Benoit J.P. Why does PEG 400 co-encapsulation improve NGF stability and release from PLGA biodegradable microspheres. Pharm. Res. 1999, 16(8):1294-1299.
7. Lam X.M., Duenas E.T., Daugherty A.L., Levin N., Cleland J.L. Sustained release of recombinant human insulin-like growth factor-I for treatment of diabetes. J. Control. Release 2000, 67(2-3):281-292.
8. Frangione-Beebe M., Rose R.T., Kaumaya P.T., Schwendeman S.P. Microencapsulation of a synthetic peptide epitope for HTLV-1 in biodegradable poly(d,l-lactide-co-glycolide) microspheres using a novel encapsulation technique. J. Microencapsul. 2001, 18(5):663-677.
9. Jain R.A. The manufacturing techniques of various drug loaded biodegradable poly(lactide-co-glycolide) (PLGA) devices. Biomaterials 2000, 21(23):2475-2490.
10. Berkland C., Kim K., Pack D.W. Fabrication of PLG microspheres with precisely controlled and monodisperse size distributions. J. Control. Release 2001, 73(1):59-74.
11. Leo E., Ruozi B., Tosi G., Vandelli M.A. PLA-microparticles formulated by means a thermoreversible gel able to modify protein encapsulation and release without being co-encapsulated. Int. J. Pharm. 2006, 323(1-2):131-138.
12. Katare Y.K., Panda A.K. Influences of excipients on in vitro release and in vivo performance of tetanus toxoid loaded polymer particles. Eur. J. Pharm. Sci. 2006, 28(3):179-188.
13. Ruan G., Feng S.S., Li Q.T. Effects of material hydrophobicity on physical properties of polymeric microspheres formed by double emulsion process. J. Control. Release 2002, 84(3):151-160.
14. Jiang G., Thanoo B.C., DeLuca P.P. Effect of osmotic pressure in the solvent extraction phase on BSA release profile from PLGA microspheres. Pharm. Dev. Technol. 2002, 7(4):391-399.
15. Crotts G.P., T Preparation of porous and nonporous biodegradable polymeric hollow microshperes. J. Control. Release 1995, 35:91-105.
16. Tamber H., Johansen P., Merkle H.P., Gander B. Formulation aspects of biodegradable polymeric microspheres for antigen delivery. Adv. Drug Deliv. Rev. 2005, 57(3):357-376.
17. Liu R., Ma G.H., Wan Y.H., Su Z.G. Influence of process parameters on the size distribution of PLA microcapsules prepared by combining membrane emulsification technique and double emulsion-solvent evaporation method. Colloids Surf. B Biointerfaces 2005, 45(3-4):144-153.
18. Liu R., Huang S.S., Wan Y.H., Ma G.H., Su Z.G. Preparation of insulin-loaded PLA/PLGA microcapsules by a novel membrane emulsification method and its release in vitro. Colloids Surf. B Biointerfaces 2006, 51(1):30-38.
19. Ito F., Fujimori H., Makino K. Incorporation of water-soluble drugs in PLGA microspheres. Colloids Surf. B Biointerfaces 2007, 54(2):173-178.
20. van de Weert M., Hoechstetter J., Hennink W.E., Crommelin D.J. The effect of a water/organic solvent interface on the structural stability of lysozyme. J. Control. Release 2000, 68(3):351-359.
21. Castellanos I.J., Cruz G., Crespo R., Griebenow K. Encapsulation-induced aggregation and loss in activity of gamma-chymotrypsin and their prevention. J. Control. Release 2002, 81(3):307-319.
22. Wang J., Chua K.M., Wang C.H. Stabilization and encapsulation of human immunoglobulin G into biodegradable microspheres. J. Colloid. Interface Sci. 2004, 271(1):92-101.
23. Castellanos I.J., Crespo R., Griebenow K. Poly(ethylene glycol) as stabilizer and emulsifying agent: a novel stabilization approach preventing aggregation and inactivation of proteins upon encapsulation in bioerodible polyester microspheres. J. Control. Release 2003, 88(1):135-145.
24. Castellanos I.J., Griebenow K. Improved alpha-chymotrypsin stability upon encapsulation in PLGA microspheres by solvent replacement. Pharm. Res. 2003, 20(11):1873-1880.
25. Cleland J.L., Jones A.J. Stable formulations of recombinant human growth hormone and interferon-gamma for microencapsulation in biodegradable microspheres. Pharm. Res. 1996, 13(10):1464-1475.
26. Costantino H.R., Firouzabadian L., Hogeland K., Wu C., Beganski C., Carrasquillo K.G., Cordova M., Griebenow K., Zale S.E., Tracy M.A. Protein spray-freeze drying. Effect of atomization conditions on particle size and stability. Pharm. Res. 2000, 17(11):1374-1383.
27. Bao W., Zhou J., Luo J., Wu D. PLGA microspheres with high drug loading and high encapsulation efficiency prepared by a novel solvent evaporation technique. J. Microencapsul. 2006, 23(5):471-479.
28. Kostanski J.W., Thanoo B.C., DeLuca P.P. Preparation, characterization, and in vitro evaluation of 1- and 4-month controlled release orntide PLA and PLGA microspheres. Pharm. Dev. Technol. 2000, 5(4):585-596.
29. Woo B.H., Kostanski J.W., Gebrekidan S., Dani B.A., Thanoo B.C., DeLuca P.P. Preparation, characterization and in vivo evaluation of 120-day poly(d, l-lactide) leuprolide microspheres. J. Control. Release 2001, 75(3):307-315.
30. Sandor M., Riechel A., Kaplan I., Mathiowitz E. Effect of lecithin and MgCO3 as additives on the enzymatic activity of carbonic anhydrase encapsulated in poly(lactide-co-glycolide) (PLGA) microspheres. Biochim. Biophys. Acta 2002, 1570(1):63-74.
31. Cleland J.L. Protein Delivery: Physical Systems 1997, Vol. 10:1-43. Plenum Press, New York. L.M. Sanders, R.W. Hendren (Eds.).
32. Thomasin C., Ho N.T., Merkle H.P., Gander B. Drug microencapsulation by PLA/PLGA coacervation in the light of thermodynamics. 1. Overview and theoretical considerations. J. Pharm. Sci. 1998, 87(3):259-268.
33. Ciombor D.M., Jaklenec A., Liu A.Z., Thanos C., Rahman N., Weston P., Aaron R., Mathiowitz E. Encapsulation of BSA using a modified W/O/O emulsion solvent removal method. J. Microencapsul. 2006, 23(2):183-194.
34. Thomasin C., Merkle H.P., Gander B. Drug microencapsulation by PLA/PLGA coacervation in the light of thermodynamics. 2. Parameters determining microsphere formation. J. Pharm. Sci. 1998, 87(3):269-275.
35. Blanco-Prieto M.J., Campanero M.A., Besseghir K., Heimgatner F., Gander B. Importance of single or blended polymer types for controlled in vitro release and plasma levels of a somatostatin analogue entrapped in PLA/PLGA microspheres. J. Control. Release 2004, 96(3):437-448.
36. Carrasquillo K.G., Stanley A.M., Aponte-Carro J.C., De Jesus P., Costantino H.R., Bosques C.J., Griebenow K. Non-aqueous encapsulation of excipient-stabilized spray-freeze dried BSA into poly(lactide-co-glycolide) microspheres results in release of native protein. J. Control. Release 2001, 76(3):199-208.
37. Tobio M., Nolley J., Guo Y., McIver J., Alonso M.J. A novel system based on a poloxamer/PLGA blend as a tetanus toxoid delivery vehicle. Pharm. Res. 1999, 16(5):682-688.
38. Leach W.T., Simpson D.T., Val T.N., Yu Z., Lim K.T., Park E.J., Williams R.O., Johnston K.P. Encapsulation of protein nanoparticles into uniform-sized microspheres formed in a spinning oil film. AAPS Pharm. Sci. Tech. 2005, 6(4):E605-E617.
39. Giunchedi P., Conti B., Genta I., Conte U., Puglisi G. Emulsion spray-drying for the preparation of albumin-loaded PLGA microspheres. Drug Dev. Ind. Pharm. 2001, 27(7):745-750.
40. Freitas S., Merkle H.P., Gander B. Ultrasonic atomisation into reduced pressure atmosphere-envisaging aseptic spray-drying for microencapsulation. J. Control. Release 2004, 95(2):185-195.
41. Quaglia F., De Rosa G., Granata E., Ungaro F., Fattal E., Immacolata La Rotonda M. Feeding liquid, non-ionic surfactant and cyclodextrin affect the properties of insulin-loaded poly(lactide-co-glycolide) microspheres prepared by spray-drying. J. Control. Release 2003, 86(2-3):267-278.
42. De Rosa G., Larobina D., Immacolata La Rotonda M., Musto P., Quaglia F., Ungaro F. How cyclodextrin incorporation affects the properties of protein-loaded PLGA-based microspheres: the case of insulin/hydroxypropyl-beta-cyclodextrin system. J. Control. Release 2005, 102(1):71-83.
43. Johansen P., Men Y., Audran R., Corradin G., Merkle H.P., Gander B. Improving stability and release kinetics of microencapsulated tetanus toxoid by co-encapsulation of additives. Pharm. Res. 1998, 15(7):1103-1110.
44. Johansen P., Tamber H., Merkle H.P., Gander B. Diphtheria and tetanus toxoid microencapsulation into conventional and end-group alkylated PLA/PLGAs. Eur. J. Pharm. Biopharm. 1999, 47(3):193-201.
45. Blanco-Prieto M.J., Besseghir K., Zerbe O., Andris D., Orsolini P., Heimgartner F., Merkle H.P., Gander B. In vitro and in vivo evaluation of a somatostatin analogue released from PLGA microspheres. J. Control. Release 2000, 67(1):19-28.
46. Bittner B., Morlock M., Koll H., Winter G., Kissel T. Recombinant human erythropoietin (rhEPO) loaded poly(lactide-co-glycolide) microspheres: influence of the encapsulation technique and polymer purity on microsphere characteristics. Eur. J. Pharm. Biopharm. 1998, 45(3):295-305.
47. Costantino H.R., Johnson O.L., Zale S.E. Relationship between encapsulated drug particle size and initial release of recombinant human growth hormone from biodegradable microspheres. J. Pharm. Sci. 2004, 93(10):2624-2634.
48. Johnson O.L., Jaworowicz W., Cleland J.L., Bailey L., Charnis M., Duenas E., Wu C., Shepard D., Magil S., Last T., Jones A.J., Putney S.D. The stabilization and encapsulation of human growth hormone into biodegradable microspheres. Pharm. Res. 1997, 14(6):730-735.
49. Jones A.J., Putney S., Johnson O.L., Cleland J.L. Recombinant human growth hormone poly(lactic-co-glycolic acid) microsphere formulation development. Adv. Drug Deliv. Rev. 1997, 28(1):71-84.
50. Lam X.M., Duenas E.T., Cleland J.L. Encapsulation and stabilization of nerve growth factor into poly(lactic-co-glycolic) acid microspheres. J. Pharm. Sci. 2001, 90(9):1356-1365.
51. Cleland J.L., Duenas E.T., Park A., Daugherty A., Kahn J., Kowalski J., Cuthbertson A. Development of poly-(d,l-lactide-coglycolide) microsphere formulations containing recombinant human vascular endothelial growth factor to promote local angiogenesis. J. Control. Release 2001, 72(1-3):13-24.
52. [52] W. Gombotz, M. Healy, L. Brown, Very low temperature casting of controlled release microspheres, U.S. Patent 5,019,400, May 28, 1991.
53. Berkland C., Pollauf E., Varde N., Pack D.W., Kim K.K. Monodisperse liquid-filled biodegradable microcapsules. Pharm. Res. 2007, 24(5):1007-1013.
54. Berkland C., King M., Cox A., Kim K., Pack D.W. Precise control of PLG microsphere size provides enhanced control of drug release rate. J. Control. Release 2002, 82(1):137-147.
55. Berkland C., Pack D.W., Kim K.K. Controlling surface nano-structure using flow-limited field-injection electrostatic spraying (FFESS) of poly(d,l-lactide-co-glycolide). Biomaterials 2004, 25(25):5649-5658.
56. Freitas S., Rudolf B., Merkle H.P., Gander B. Flow-through ultrasonic emulsification combined with static micromixing for aseptic production of microspheres by solvent extraction. Eur. J. Pharm. Biopharm. 2005, 61(3):181-187.
57. Freitas S., Hielscher G., Merkle H.P., Gander B. Continuous contact- and contamination-free ultrasonic emulsification-a useful tool for pharmaceutical development and production. Ultrason. Sonochem. 2006, 13(1):76-85.
58. Freitas S., Merkle H.P., Gander B. Microencapsulation by solvent extraction/evaporation: reviewing the state of the art of microsphere preparation process technology. J. Control. Release 2005, 102(2):313-332.
59. Freitas S., Walz A., Merkle H.P., Gander B. Solvent extraction employing a static micromixer: a simple, robust and versatile technology for the microencapsulation of proteins. J. Microencapsul. 2003, 20(1):67-85.
60. Yeo Y., Basaran O.A., Park K. A new process for making reservoir-type microcapsules using ink-jet technology and interfacial phase separation. J. Control. Release 2003, 93(2):161-173.
61. Yeo Y., Chen A.U., Basaran O.A., Park K. Solvent exchange method: a novel microencapsulation technique using dual microdispensers. Pharm. Res. 2004, 21(8):1419-1427.
62. Yeo Y., Park K. A new microencapsulation method using an ultrasonic atomizer based on interfacial solvent exchange. J. Control. Release 2004, 100(3):379-388.
63. Felder Ch B., Blanco-Prieto M.J., Heizmann J., Merkle H.P., Gander B. Ultrasonic atomization and subsequent polymer desolvation for peptide and protein microencapsulation into biodegradable polyesters. J. Microencapsul. 2003, 20(5):553-567.
64. Park J.H., Ye M., Yeo Y., Lee W.K., Paul C., Park K. Reservoir-type microcapsules prepared by the solvent exchange method: effect of formulation parameters on microencapsulation of lysozyme. Mol. Pharm. 2006, 3(2):135-143.
65. Yeo Y., Park K. Characterization of reservoir-type microcapsules made by the solvent exchange method. AAPS Pharm. Sci. Tech. 2004, 5(4):e52.
66. Fenn J.B., Mann M., Meng C.K., Wong S.F., Whitehouse C.M. Electrospray ionization for mass spectrometry of large biomolecules. Science 1989, 246(4926):64-71.
67. Loscertales I.G., Barrero A., Guerrero I., Cortijo R., Marquez M., Ganan-Calvo A.M. Micro/nano encapsulation via electrified coaxial liquid jets. Science 2002, 295(5560):1695-1698.
68. Xu Y., Hanna M.A. Electrospray encapsulation of water-soluble protein with polylactide. Effects of formulations on morphology, encapsulation efficiency and release profile of particles. Int. J. Pharm. 2006, 320(1-2):30-36.
69. Xu Y., Skotak M., Hanna M. Electrospray encapsulation of water-soluble protein with polylactide. I. Effects of formulations and process on morphology and particle size. J. Microencapsul. 2006, 23(1):69-78.
70. Gomez A., Bingham D., de Juan L., Tang K. Production of protein nanoparticles by electrospray drying. J. Aerosol Sci. 1998, 29(5-6):561-574.
71. Kuo S., Niu G., Chang S., Kuo C., Bair M. A one-step method for fabricating chitosan microspheres. J. Appl. Pol. Sci. 2004, 94(5):2150-2157.
72. Xie J., Wang C.H. Encapsulation of proteins in biodegradable polymeric microparticles using electrospray in the Taylor cone-jet mode. Biotechnol. Bioeng. 2007, 97(5):1278-1290.
73. Tan Y.C., Hettiarachchi K., Siu M., Pan Y.R., Lee A.P. Controlled microfluidic encapsulation of cells, proteins, and microbeads in lipid vesicles. J. Am. Chem. Soc. 2006, 128(17):5656-5658.
74. Okushima S., Nisisako T., Torii T., Higuchi T. Controlled production of monodisperse double emulsions by two-step droplet breakup in microfluidic devices. Langmuir 2004, 20(23):9905-9908.
75. Joanicot M., Ajdari A. Applied physics. Droplet control for microfluidics. Science 2005, 309(5736):887-888.
76. Nisisako T., Shingo Okushima S., Torii T. Controlled formulation of monodisperse double emulsions in a multiple-phase microfluidic system. Soft Matter. 2005, 1(1):23-27.
77. Takeuchi S., Garstecki P., Weibel D., Whitesides G. An axisymmetric flow-focusing microfluidic device. Adv. Mater. 2005, 17(8):1067-1072.
78. Nie Z., Xu S., Seo M., Lewis P.C., Kumacheva E. Polymer particles with various shapes and morphologies produced in continuous microfluidic reactors. J. Am. Chem. Soc. 2005, 127(22):8058-8063.
79. Lorenceau E., Utada A.S., Link D.R., Cristobal G., Joanicot M., Weitz D.A. Generation of polymerosomes from double-emulsions. Langmuir 2005, 21(20):9183-9186.
80. Utada A.S., Lorenceau E., Link D.R., Kaplan P.D., Stone H.A., Weitz D.A. Monodisperse double emulsions generated from a microcapillary device. Science 2005, 308(5721):537-541.
81. Zhang H., Tumarkin E., Peerani R., Nie Z., Sullan R.M., Walker G.C., Kumacheva E. Microfluidic production of biopolymer microcapsules with controlled morphology. J. Am. Chem. Soc. 2006, 128(37):12205-12210.
82. Kim H.K., Chung H.J., Park T.G. Biodegradable polymeric microspheres with "open/closed" pores for sustained release of human growth hormone. J. Control. Release 2006, 112(2):167-174.
83. Rolland J.P., Maynor B.W., Euliss L.E., Exner A.E., Denison G.M., DeSimone J.M. Direct fabrication and harvesting of monodisperse, shape-specific nanobiomaterials. J. Am. Chem. Soc. 2005, 127:10096-10100.
84. Gratton S.E.A., Pohlhaus P.D., Lee J., Guo J., Cho M.J., DeSimone J.M. Nanofabricated particles for engineered drug therapies: a preliminary biodistribution study of PRINT™ nanoparticles. J. Control. Release 2007, 121:10-18.
85. Kelly J.Y., DeSimone J.M. Shape-specific, monodisperse nano-molding of protein particles. J. Am. Chem. Soc. 2008, 130:5438-5439.
86. Petros R.A., Ropp P.A., DeSimone J.M. Reductively labile PRINT particles for the delivery of doxorubicin to HeLa cells. J. Am. Chem. Soc. 2008, 130:5008-5009.
87. Guan J., Chakrapani A., Hansford D.J. Polymer microparticles fabricated by soft lithography. Chem. Mater. 2005, 17:6227-6229.
88. Glangchai L.C., Caldorera-Moore M., Shi L., Roy K. Nanoimprint lithography based fabrication of shape-specific, enzymatically-triggered smart nanoparticles. J. Control. Release 2008, 125:263-272.
89. Acharya G., Shin C.S., McDermott M., Mishra H., Park H., Kwon I.C., Park K. The hydrogel template method for fabrication of homogeneous nano/microparticles. J. Control. Release 2010, 141:314-319.
90. Kang J., Schwendeman S.P. Pore closing and opening in biodegradable polymers and their effect on the controlled release of proteins. Mol. Pharm. 2007, 4(1):104-118.
91. Bouissou C., Rouse J.J., Price R., van der Walle C.F. The influence of surfactant on PLGA microsphere glass transition and water sorption: remodeling the surface morphology to attenuate the burst release. Pharm. Res. 2006, 23(6):1295-1305.
92. Brunner A., Mader K., Gopferich A. pH and osmotic pressure inside biodegradable microspheres during erosion. Pharm. Res. 1999, 16(6):847-853.
93. Jaganathan K.S., Rao Y.U., Singh P., Prabakaran D., Gupta S., Jain A., Vyas S.P. Development of a single dose tetanus toxoid formulation based on polymeric microspheres: a comparative study of poly(d,l-lactic-co-glycolic acid) versus chitosan microspheres. Int. J. Pharm. 2005, 294(1-2):23-32.
94. Chung T.W., Tsai Y.L., Hsieh J.H., Tsai W.J. Different ratios of lactide and glycolide in PLGA affect the surface property and protein delivery characteristics of the PLGA microspheres with hydrophobic additives. J. Microencapsul. 2006, 23(1):15-27.
95. Pean J.M., Venier-Julienne M.C., Boury F., Menei P., Denizot B., Benoit J.P. NGF release from poly(d,l-lactide-co-glycolide) microspheres. Effect of some formulation parameters on encapsulated NGF stability. J. Control. Release 1998, 56(1-3):175-187.
96. Chen J.L., Chiang C.H., Yeh M.K. The mechanism of PLA microparticle formation by water-in-oil-in-water solvent evaporation method. J. Microencapsul. 2002, 19(3):333-346.
97. Herrmann J.B., R The effect of particle microstructure on the somatostatin release from poly(lactide) microspheres prepared by a W/O/W solvent evaporation method. J. Control. Release 1995, 36(1-2):63-71.
98. Wei G., Pettway G.J., McCauley L.K., Ma P.X. The release profiles and bioactivity of parathyroid hormone from poly(lactic-co-glycolic acid) microspheres. Biomaterials 2004, 25(2):345-352.
99. Yang Y.Y., Chia H.H., Chung T.S. Effect of preparation temperature on the characteristics and release profiles of PLGA microspheres containing protein fabricated by double-emulsion solvent extraction/evaporation method. J. Control. Release 2000, 69(1):81-96.
100. Yang Y.Y., Chung T.S., Ng N.P. Morphology, drug distribution, and in vitro release profiles of biodegradable polymeric microspheres containing protein fabricated by double-emulsion solvent extraction/evaporation method. Biomaterials 2001, 22(3):231-241.
101. Costantino H.R., Firouzabadian L., Wu C., Carrasquillo K.G., Griebenow K., Zale S.E., Tracy M.A. Protein spray freeze drying. 2. Effect of formulation variables on particle size and stability. J. Pharm. Sci. 2002, 91(2):388-395.
102. Igartua M., Hernandez R.M., Esquisabel A., Gascon A.R., Calvo M.B., Pedraz J.L. Influence of formulation variables on the in-vitro release of albumin from biodegradable microparticulate systems. J. Microencapsul. 1997, 14(3):349-356.
103. Wischke C., Borchert H.H. Influence of the primary emulsification procedure on the characteristics of small protein-loaded PLGA microparticles for antigen delivery. J. Microencapsul. 2006, 23(4):435-448.
104. Zhu K.J., Jiang H.L., Du X.Y., Wang J., Xu W.X., Liu S.F. Preparation and characterization of hCG-loaded polylactide or poly(lactide-co-glycolide) microspheres using a modified water-in-oil-in-water (w/o/w) emulsion solvent evaporation technique. J. Microencapsul. 2001, 18(2):247-260.
105. He J.T., Su H.B., Li G.P., Tao X.M., Mo W., Song H.Y. Stabilization and encapsulation of a staphylokinase variant (K35R) into poly(lactic-co-glycolic acid) microspheres. Int. J. Pharm. 2006, 309(1-2):101-108.
106. Blanco D., Alonso M.J. Protein encapsulation and release from poly(lactide-co-glycolide) microspheres: effect of the protein and polymer properties and of the co-encapsulation of surfactants. Eur. J. Pharm. Biopharm. 1998, 45(3):285-294.
107. Castellanos I.J., Carrasquillo K.G., Lopez J.D., Alvarez M., Griebenow K. Encapsulation of bovine serum albumin in poly(lactide-co-glycolide) microspheres by the solid-in-oil-in-water technique. J. Pharm. Pharmacol. 2001, 53(2):167-178.
108. Zhang J.X., Zhu K.J., Chen D. Preparation of bovine serum albumin loaded poly (d,l-lactic-co-glycolic acid) microspheres by a modified phase separation technique. J. Microencapsul. 2005, 22(2):117-126.
109. Lee E.S., Kwon M.J., Lee H., Na K., Kim J.J. In vitro study of lysozyme in poly(lactide-co-glycolide) microspheres with sucrose acetate isobutyrate. Eur. J. Pharm. Sci. 2006, 29(5):435-441.
110. Lee E.S., Park K.H., Park I.S., Na K. Glycol chitosan as a stabilizer for protein encapsulated into poly(lactide-co-glycolide) microparticle. Int. J. Pharm. 2007, 338(1-2):310-316.
111. Perez C., De Jesus P., Griebenow K. Preservation of lysozyme structure and function upon encapsulation and release from poly(lactic-co-glycolic) acid microspheres prepared by the water-in-oil-in-water method. Int. J. Pharm. 2002, 248(1-2):193-206.
112. Lee J., Lee K.Y. Injectable microsphere/hydrogel combination systems for localized protein delivery. Macromol. Biosci. 2009, 9(7):671-676.
113. Lee J., Tan C.Y., Lee S.K., Kim Y.H., Lee K.Y. Controlled delivery of heat shock protein using an injectable microsphere/hydrogel combination system for the treatment of myocardial infarction. J. Control. Release 2009, 137(3-4):196-202.
114. Srinivasan C., Katare Y.K., Muthukumaran T., Panda A.K. Effect of additives on encapsulation efficiency, stability and bioactivity of entrapped lysozyme from biodegradable polymer particles. J. Microencapsul. 2005, 22(2):127-138.
115. Garbayo E., Ansorena E., Lanciego J.L., Aymerich M.S., Blanco-Prieto M.J. Sustained release of bioactive glycosylated glial cell-line derived neurotrophic factor from biodegradable polymeric microspheres. Eur. J. Pharm. Biopharm. 2008, 69(3):844-851.
116. Pistel K.F., Kissel T. Effects of salt addition on the microencapsulation of proteins using W/O/W double emulsion technique. J. Microencapsul. 2000, 17(4):467-483.
117. Bertram J.P., Rauch M.F., Chang K., Lavik E.B. Using polymer chemistry to modulate the delivery of neurotrophic factors from degradable microspheres: delivery of BDNF. Pharm. Res. 2010, 27(1):82-91.
118. Ho M.L., Fu Y.C., Wang G.J., Chen H.T., Chang J.K., Tsai T.H., Wang C.K. Controlled release carrier of BSA made by W/O/W emulsion method containing PLGA and hydroxyapatite. J. Control. Release 2008, 128(2):142-148.
119. Park W., Na K. Dermatan sulfate as a stabilizer for protein stability in poly(lactide-co-glycolide). Depot. Biotech. Bioproc. Eng. 2009, 14(5):668-674.
120. Park W., Na K. Polyelectrolyte complex of chondroitin sulfate and peptide with lower pI value in poly(lactide-co-glycolide) microsphere for stability and controlled release. Colloids Surf. B Biointerfaces 2009, 72(2):193-200.
121. Dong X.Q., Xu J., Wang W.C., Luo H., Liang X.F., Zhang L., Wang H.J., Wang P.H., Chang J. Repair effect of diabetic ulcers with recombinant human epidermal growth factor loaded by sustained-release microspheres. Sci. China Series C-Life Sci. 2008, 51(11):1039-1044.
122. Zhang Y.M., Yang F., Yang Y.Q., Song F.L., Xu A.L. Recombinant interferon-alpha2b poly(lactic-co-glycolic acid) microspheres: pharmacokinetics-pharmacodynamics study in rhesus monkeys following intramuscular administration. Acta Pharmacol. Sinica 2008, 29(11):1370-1375.
123. Han K., Lee K.D., Gao Z.G., Park J.S. Preparation and evaluation of poly(l-lactic acid) microspheres containing rhEGF for chronic gastric ulcer healing. J. Control. Release 2001, 75(3):259-269.
124. Ghassemi A.H., van Steenbergen M.J., Talsma H., van Nostrum C.F., Jiskoot W., Crommelin D.J., Hennink W.E. Preparation and characterization of protein loaded microspheres based on a hydroxylated aliphatic polyester, poly(lactic-co-hydroxymethyl glycolic acid). J. Control. Release 2009, 138(1):57-63.
125. Kim J.H., Taluja A., Knutson K., Han Bae Y. Stability of bovine serum albumin complexed with PEG-poly(l-histidine) diblock copolymer in PLGA microspheres. J. Control. Release 2005, 109(1-3):86-100.
126. Kirby D.J., Rosenkrands I., Agger E.M., Andersen P., Coombes A.G.A., Perrie Y. PLGA microspheres for the delivery of a novel subunit TB vaccine. J. Drug Target. 2008, 16(4):282-293.
127. Wang M.B., Feng Q.L., Niu X.F., Tan R.W., She Z.D. A spheres-in-sphere structure for improving protein-loading poly (lactide-co-glycolide) microspheres. Polym. Degrad. Stab. 2010, 95(1):6-13.
128. Yang H.J., Park I.S., Na K. Biocompatible microspheres based on acetylated polysaccharide prepared from water-in-oil-in-water (W-1/O/W-2) double-emulsion method for delivery of type II diabetic drug (exenatide). Colloids Surf. A Physicochem. Eng. Aspects 2009, 340(1-3):115-120.
129. Zhu X.H., Wang C.H., Tong Y.W. In vitro characterization of hepatocyte growth factor release from PHBV/PLGA microsphere scaffold. J. Biomed. Mater. Res. A 2009, 89A(2):411-423.
130. Igartua M., Hernandez R.M., Rosas J.E., Patarroyo M.E., Pedraz J.L. gamma-Irradiation effects on biopharmaceutical properties of PLGA microspheres loaded with SPf66 synthetic vaccine. Eur. J. Pharm. Biopharm. 2008, 69(2):519-526.
131. Kokai L.E., Tan H.P., Jhunjhunwala S., Little S.R., Frank J.W., Marra K.G. Protein bioactivity and polymer orientation is affected by stabilizer incorporation for double-walled microspheres. J. Control. Release 2010, 141(2):168-176.
132. Morita T., Sakamura Y., Horikiri Y., Suzuki T., Yoshino H. Protein encapsulation into biodegradable microspheres by a novel S/O/W emulsion method using poly(ethylene glycol) as a protein micronization adjuvant. J. Control. Release 2000, 69(3):435-444.
133. Castellanos I.J., Cuadrado W.O., Griebenow K. Prevention of structural perturbations and aggregation upon encapsulation of bovine serum albumin into poly(lactide-co-glycolide) micropheres using the solid-in-oil-in water technique. J. Pharm. Pharmacol. 2001, 53(8):1099-1107.
134. Jiang H.L., Jin J.F., Hu Y.Q., Zhu K.J. Improvement of protein loading and modulation of protein release from poly(lactide-co-glycolide) microspheres by complexation of proteins with polyanions. J. Microencapsul. 2004, 21(6):615-624.
135. Castellanos I.J., Flores G., Griebenow K. Effect of cyclodextrins on alpha-chymotrypsin stability and loading in PLGA microspheres upon S/O/W encapsulation. J. Pharm. Sci. 2006, 95(4):849-858.
136. Yuan W.E., Wu F., Guo M.Y., Jin T. Development of protein delivery microsphere system by a novel S/O/P/W multi-emulsion. Eur. J. Pharm. Sci. 2009, 36(2-3):212-218.
137. Yamaguchi Y., Takenaga M., Kitagawa A., Ogawa Y., Mizushima Y., Igarashi R. Insulin-loaded biodegradable PLGA microcapsules: initial burst release controlled by hydrophilic additives. J. Control. Release 2002, 81(3):235-249.
138. Schoubben A., Blasi P., Giovagnoli S., Perioli L., Rossi C., Ricci M. Novel composite microparticles for protein stabilization and delivery. Eur. J. Pharm. Sci. 2009, 36(2-3):226-234.
139. Emami J., Hamishehkar H., Najafabadi A.R., Gilani K., Minaiyan M., Mahdavi H., Nokhodchi A. A novel approach to prepare insulin-loaded poly (lactic-co-glycolic acid) microcapsules and the protein stability study. J. Pharm. Sci. 2009, 98(5):1712-1731.
140. Jain R.A., Rhodes C.T., Railkar A.M., Malick A.W., Shah N.H. Comparison of various injectable protein-loaded biodegradable poly(lactide-co-glycolide) (PLGA) devices: in-situ-formed implant versus in-situ-formed microspheres versus isolated microspheres. Pharm. Dev. Technol. 2000, 5(2):201-207.
141. Han Y.D., Tian H.Y., He P., Chen X.S., Jing X.B. Insulin nanoparticle preparation and encapsulation into poly(lactic-co-glycolic acid) microspheres by using an anhydrous system. Int. J. Pharm. 2009, 378(1-2):159-166.
142. Wu J.H., Ding D.W., Ren G.Y., Xu X.Y., Yin X.J., Hu Y.Q. Sustained delivery of endostatin improves the efficacy of therapy in Lewis lung cancer model. J. Control. Release 2009, 134(2):91-97.
143. Wu J.H., Wu L., Xu X.Q., Xu X.Y., Yin X.J., Chen Y.J., Hu Y.Q. Microspheres made by W/O/O emulsion method with reduced initial burst for long-term delivery of endostar, a novel recombinant human endostatin. J. Pharm. Sci. 2009, 98(6):2051-2058.
144. Hamishehkar H., Emami J., Najafabadi A.R., Gilani K., Minaiyan M., Mahdavi H., Nokhodchi A. The effect of formulation variables on the characteristics of insulin-loaded poly(lactic-co-glycolic acid) microspheres prepared by a single phase oil in oil solvent evaporation method. Colloids Surf. B Biointerfaces 2009, 74(1):340-349.
145. Yin D.F., Lu Y., Zhang H., Zhang G.Q., Zou H., Sun D.X., Zhong Y.Q. Preparation of glucagon-like peptide-1 loaded PLGA microspheres: characterizations, release studies and bioactivities in vitro/in vivo. Chem. Pharm. Bull. 2008, 56(2):156-161.
146. Jordan F., Naylor A., Kelly C.A., Howdle S.M., Lewis A., Illum L. Sustained release hGH microsphere formulation produced by a novel supercritical fluid technology: in vivo studies. J. Control. Release 2010, 141(2):153-160.
147. Rosa G.D., Iommelli R., La Rotonda M.I., Miro A., Quaglia F. Influence of the co-encapsulation of different non-ionic surfactants on the properties of PLGA insulin-loaded microspheres. J. Control. Release 2000, 69(2):283-295.
148. Nihant N., Schugens C., Grandfils C., Jerome R., Teyssie P. Polylactide microparticles prepared by double emulsion/evaporation technique. I. Effect of primary emulsion stability. Pharm. Res. 1994, 11(10):1479-1484.
149. Cho M., Sah H. Formulation and process parameters affecting protein encapsulation into PLGA microspheres during ethyl acetate-based microencapsulation process. J. Microencapsul. 2005, 22(1):1-12.
150. van de Weert M., Hennink W.E., Jiskoot W. Protein instability in poly(lactic-co-glycolic acid) microparticles. Pharm. Res. 2000, 17(10):1159-1167.
151. Meinel L., Illi O.E., Zapf J., Malfanti M., Peter Merkle H., Gander B. Stabilizing insulin-like growth factor-I in poly(d,l-lactide-co-glycolide) microspheres. J. Control. Release 2001, 70(1-2):193-202.
152. Perez C., Griebenow K. Improved activity and stability of lysozyme at the water/CH2Cl2 interface: enzyme unfolding and aggregation and its prevention by polyols. J. Pharm. Pharmacol. 2001, 53(9):1217-1226.
153. Perez-Rodriguez C., Montano N., Gonzalez K., Griebenow K. Stabilization of alpha-chymotrypsin at the CH2Cl2/water interface and upon water-in-oil-in-water encapsulation in PLGA microspheres. J. Control. Release 2003, 89(1):71-85.
154. Determan A.S., Wilson J.H., Kipper M.J., Wannemuehler M.J., Narasimhan B. Protein stability in the presence of polymer degradation products: consequences for controlled release formulations. Biomaterials 2006, 27(17):3312-3320.
155. Tracy M.A. Development and scale-up of a microsphere protein delivery system. Biotechnol. Prog. 1998, 14(1):108-115.
156. Zhu G., Schwendeman S.P. Stabilization of proteins encapsulated in cylindrical poly(lactide-co-glycolide) implants: mechanism of stabilization by basic additives. Pharm. Res. 2000, 17(3):351-357.
157. Lagarce F., Garcion E., Faisant N., Thomas O., Kanaujia P., Menei P., Benoit J.P. Development and characterization of interleukin-18-loaded biodegradable microspheres. Int. J. Pharm. 2006, 314(2):179-188.
158. Castellanos I.J., Flores G., Griebenow K. Effect of the molecular weight of poly(ethylene glycol) used as emulsifier on alpha-chymotrypsin stability upon encapsulation in PLGA microspheres. J. Pharm. Pharmacol. 2005, 57(10):1261-1269.
159. Morita T., Horikiri Y., Yamahara H., Suzuki T., Yoshino H. Formation and isolation of spherical fine protein microparticles through lyophilization of protein-poly(ethylene glycol) aqueous mixture. Pharm. Res. 2000, 17(11):1367-1373.
160. Bartus R.T., Tracy M.A., Emerich D.F., Zale S.E. Sustained delivery of proteins for novel therapeutic agents. Science 1998, 281(5380):1161-1162.
161. Takenaga M., Yamaguchi Y., Kitagawa A., Ogawa Y., Mizushima Y., Igarashi R. A novel sustained-release formulation of insulin with dramatic reduction in initial rapid release. J. Control. Release 2002, 79(1-3):81-91.
162. Chornet E., Dumitriu S. Inclusion and release of proteins from polysaccharide-based polyion complexes. Adv. Drug Deliv. Rev. 1998, 31(3):223-246.
163. Schwendeman S.P., Tobio M., Joworowicz M., Alonso M.J., Langer R. New strategies for the microencapsulation of tetanus vaccine. J. Microencapsul. 1998, 15(3):299-318.
164. Tobio M., Schwendeman S.P., Guo Y., McIver J., Langer R., Alonso M.J. Improved immunogenicity of a core-coated tetanus toxoid delivery system. Vaccine 2000, 18(7):618-622.
165. Nielsen H.M., Jorgensen L. Delivery Technologies for Biopharmaceuticals. Peptides, Proteins, Nucleic Acids and Vaccines 2009, John Wiley & Sons, Chippenham, Wiltshire, Great Britain. L. Jorgensen, H.M. Nielsen (Eds.).
166. Weert M.V.D. Delivery technologies for biopharmaceuticals. Peptides, Proteins, Nucleic Acids and Vaccines 2009, 407-412. John Wiley & Sons, Chippenham, Wiltshire, Great Britain. L. Jorgensen, H.M. Nielsen (Eds.).
167. Callewaert M., Laurent-Maquin D., Edwards-Levy F. Albumin-alginate-coated microspheres: resistance to steam sterilization and to lyophilization. Int. J. Pharm. 2007, 344(1-2):161-164.
168. Athanasiou K.A., Niederauer G.G., Agrawal C.M. Sterilization, toxicity, biocompatibility and clinical applications of polylactic acid/polyglycolic acid copolymers. Biomaterials 1996, 17(2):93-102.
169. Igartua M., Hernandez R.M., Rosas J.E., Patarroyo M.E., Pedraz J.L. Gamma-irradiation effects on biopharmaceutical properties of PLGA microspheres loaded with SPf66 synthetic vaccine. Eur. J. Pharm. Biopharm. 2008, 69(2):519-526.
170. Dorati R., Patrini M., Perugini P., Pavanetto F., Stella A., Modena T., Genta I., Conti B. Surface characterization by atomic force microscopy of sterilized PLGA microspheres. J. Microencapsul. 2006, 23(2):123-133.
171. Williams H.E., Huxley J., Claybourn M., Booth J., Hobbs M., Meehan E., Clark B. The effect of γ-irradiation and polymer composition on the stability of PLG polymer and microspheres. Polym. Degrad. Stab. 2006, 91:2171-2181.
172. Montanari L., Cilurzo F., Conti B., Genta I., Groppo A., Valvo L., Faucitano A., Buttafava A. Gamma irradiation effects and EPR investigation on poly(lactide-co-glycolide) microspheres containing bupivacaine. Farmaco 2002, 57(6):427-433.
173. Carrascosa C., Espejo L., Torrado S., Torrado J.J. Effect of gamma-sterilization process on PLGA microspheres loaded with insulin-like growth factor-I (IGF-I). J. Biomater. Appl. 2003, 18(2):95-108.
174. Montanari L., Cilurzo F., Selmin F., Conti B., Genta I., Poletti G., Orsini F., Valvo L. Poly(lactide-co-glycolide) microspheres containing bupivacaine: comparison between gamma and beta irradiation effects. J. Control. Release 2003, 90(3):281-290.
175. Dillow A.K., Dehghani F., Hrkach J.S., Foster N.R., Langer R. Bacterial inactivation by using near- and supercritical carbon dioxide. Proc. Natl. Acad. Sci. U. S. A. 1999, 96(18):10344-10348.
176. Toguchi H. Sterility assurance of microspheres. J. Control. Release 1999, 62(1-2):51-55.
177. O'Hagan D.T., McGee J.P., Boyle D., Gumaer D., Li X.M., Potts B., Wang C.Y., Koff W.C. The preparation, characterization and pre-clinical evaluation of an orally administered HIV-1 vaccine, consisting of branched peptide immunogen entrapped in controlled release microparticles. J. Control. Release 1995, 36:75-84.
178. [178] ClinicalTrials.gov. A Phase I/II Safety and Immunogenicity Trial of UBI Microparticulate Monovalent (HIV-1 MN) Branched Peptide Vaccine in HIV-1 Seronegative Human Subjects., (2005), http://clinicaltrials.gov/ct2/show/NCT00002428.
179. Ishikawa E., Tsuboi K., Yamamoto T., Muroi A., Takano S., Enomoto T., Matsumura A., Ohno T. Clinical trial of autologous formalin-fixed tumor vaccine for glioblastoma multiforme patients. Cancer Sci. 2007, 98(8):1226-1233.
180. Peng B.G., Liu S.Q., Kuang M., He Q., Totsuka S., Huang L., Huang J., Lu M.D., Liang L.J., Leong K.W., Ohno T. Autologous fixed tumor vaccine: a formulation with cytokine-microparticles for protective immunity against recurrence of human hepatocellular carcinoma. Jpn. J. Cancer Res. 2002, 93(4):363-368.
181. Kuang M., Peng B.G., Lu M.D., Liang L.J., Huang J.F., He Q., Hua Y.P., Totsuka S., Liu S.Q., Leong K.W., Ohno T. Phase II randomized trial of autologous formalin-fixed tumor vaccine for postsurgical recurrence of hepatocellular carcinoma. Clin. Cancer Res. 2004, 10(5):1574-1579.
182. Vlugt-Wensink K.D., de Vrueh R., Gresnigt M.G., Hoogerbrugge C.M., van Buul-Offers S.C., de Leede L.G., Sterkman L.G., Crommelin D.J., Hennink W.E., Verrijk R. Preclinical and clinical in vitro in vivo correlation of an hGH dextran microsphere formulation. Pharm. Res. 2007, 24(12):2239-2248.