Controlled, pulsatile release of thermostabilized inactivated polio vaccine from PLGA-based microspheres
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1 Engineering Conferences International ECI Digital Archives Vaccine Technology VI Proceedings Controlled, pulsatile release of thermostabilized inactivated polio vaccine from PLGA-based microspheres Stephany Y. Tzeng Massachusetts Institute of Technology, Rohiverth Guarecuco Massachusetts Institute of Technology Kevin J. McHugh Massachusetts Institute of Technology Evan M. Rosenberg Massachusetts Institute of Technology Yingying Zeng Massachusetts Institute of Technology See next page for additional authors Follow this and additional works at: Part of the Engineering Commons Recommended Citation Stephany Y. Tzeng, Rohiverth Guarecuco, Kevin J. McHugh, Evan M. Rosenberg, Yingying Zeng, Robert Langer, and Ana Jaklenec, "Controlled, pulsatile release of thermostabilized inactivated polio vaccine from PLGA-based microspheres" in "Vaccine Technology VI", Laura Palomares, UNAM, Mexico Manon Cox, Protein Sciences Corporation, USA Tarit Mukhopadhyay, University College London, UK Nathalie Garçon, BIOASTER Technology Research Institute, FR Eds, ECI Symposium Series, (216). This Abstract and Presentation is brought to you for free and open access by the Proceedings at ECI Digital Archives. It has been accepted for inclusion in Vaccine Technology VI by an authorized administrator of ECI Digital Archives. For more information, please contact
2 Authors Stephany Y. Tzeng, Rohiverth Guarecuco, Kevin J. McHugh, Evan M. Rosenberg, Yingying Zeng, Robert Langer, and Ana Jaklenec This abstract and presentation is available at ECI Digital Archives:
3 Controlled, pulsatile release of stable inactivated polio vaccine from PLGA-based microspheres Stephany Y. Tzeng Jaklenec group, Langer Lab Massachusetts Institute of Technology June 13, 216
4 Inactivated polio vaccine (IPV): background Poliomyelitis is a potentially fatal infectious disease that can be prevented by vaccination For vaccine efficacy, IPV must be administered in 2-3 bolus injections (IM) spread over weeks or months Vaccine coverage is hampered in developing countries by difficulties of patient access in at-risk populations McHugh et al J Control Release 219:596!
5 Poly(lactic-co-glycolic acid) (PLGA) microparticles for controlled release Biodegradable polyester Hydrolytically cleaved at ester linkages Bulk-degrading Degradation rate depends on lactide-to-glycolide ratio, molecular weight, and formulation parameters Polymer degradation leads to protein release IPV encapsulated in PLGA matrix Burst #1: IPV near surface (diffusion) Burst #2: PLGA degrades and forms pores that allow IPV release Pulsatile release at relevant time points can be measured from microspheres loaded with stable antigens
6 Poly(lactic-co-glycolic acid) (PLGA) microparticles for controlled release Biodegradable polyester Hydrolytically cleaved at ester linkages Bulk-degrading Degradation rate depends on lactide-to-glycolide ratio, molecular weight, and formulation parameters Polymer degradation leads to protein release All 3 serotypes of IPV must survive encapsulation, incubation, and release without denaturation
7 Poly(lactic-co-glycolic acid) (PLGA) microparticles for controlled release Biodegradable polyester Hydrolytically cleaved at ester linkages Bulk-degrading Degradation rate depends on lactide-to-glycolide ratio, molecular weight, and formulation parameters Polymer degradation leads to protein release All 3 serotypes of IPV must survive encapsulation, incubation, and release without denaturation IPV must survive in antigenic conformation for weeks/months
8 IPV stability: thermostability 1 Stability at 37 o C Time (days) Type I Type II Type III - IPV consists of three serotypes (types 1, 2, and 3), which have different stability properties - Recovery was calculated from the D-antigenicity as measured by ELISA - IPV was incubated at 37 o C in PBS (ph 7.4) buffer - IPV is unstable at elevated temperatures, with >5% of serotype 1 denatured after 1 week at 37 o C. - All initial thermostability studies were done with IPV in aqueous solution (not in microspheres)
9 Types of excipients Sugar Protein Amino acid(s) Ions ph modulator Other Sorbitol Gelatin MSG (glutamate) MgCl 2 Mg(OH) 2 D 2 O Sucrose BSA Arginine Mg(CO) 3 Trehalose Casein Lysine Arginine Maltodextrin Methionine EPO Inulin Chitin/chitosan Aspartate Glutathione Vaccine formulations often contain a mixture of multiple excipients. Some of these are remnants of the cell culture used for vaccine production, some are added deliberately to preserve stability, and some are a combination of the above.
10 IPV stability: incubation at 37 o C 1 Stability after 28 days of incubation at 37 o C: Type 1 only 1 Stability after 28 days of incubation at 37 o C: Type 1 only No excipient Sorbitol Sorbitol+MSG Sucrose+MSG+MgCl 2 Sucrose Sucrose+MSG Sorbitol+MSG+MgCl 2 Trehalose Trehalose+MSG Trahalose+MSG+MgCl 2 Maltodextrin Maltodextrin+MSG Maltodextrin+MSG+MgCl 2 MSG+MgCl 2 No excipient 27% Sorbitol+MSG+MgCl 2 5% Sorbitol+MSG+MgCl 2 11% Sorbitol+MSG+MgCl 2 27% Sucrose+MSG+MgCl 2 11% Sucrose+MSG+MgCl 2 5% Sucrose+MSG+MgCl 2 11% Trehalose+MSG+MgCl 2 27% Trehalose+MSG+MgCl 2 5% Trehalose+MSG+MgCl 2 27% Maltodextrin+MSG+MgCl 2 5% Maltodextrin+MSG+MgCl 2 1% Gelatin 11% Maltodextrin+MSG+MgCl 2 Sugars on their own did not confer improved stability on IPV during incubation at 37 o C. Sugars performed better when combined with MSG and MgCl 2 and also performed better at higher concentrations. Of the sugars tested, maltodextrin and sucrose were the best. Tzeng et al J Control Release 233:11
11 IPV stability: incubation at 37 o C 1 Stability after 28 days of incubation at 37 o C: Type 1 only 1 Stability after 28 days of incubation at 37 o C: Type 1 only No excipient Sorbitol Sorbitol+MSG Sucrose+MSG+MgCl 2 Sucrose Sucrose+MSG Sorbitol+MSG+MgCl 2 Trehalose Trehalose+MSG Trahalose+MSG+MgCl 2 Maltodextrin Maltodextrin+MSG Maltodextrin+MSG+MgCl 2 MSG+MgCl 2 No excipient 27% Sorbitol+MSG+MgCl 2 5% Sorbitol+MSG+MgCl 2 11% Sorbitol+MSG+MgCl 2 27% Sucrose+MSG+MgCl 2 11% Sucrose+MSG+MgCl 2 5% Sucrose+MSG+MgCl 2 11% Trehalose+MSG+MgCl 2 27% Trehalose+MSG+MgCl 2 5% Trehalose+MSG+MgCl 2 27% Maltodextrin+MSG+MgCl 2 5% Maltodextrin+MSG+MgCl 2 1% Gelatin 11% Maltodextrin+MSG+MgCl 2 Sugars on their own did not confer improved stability on IPV during incubation at 37 o C. Sugars performed better when combined with MSG and MgCl 2 and also performed better at higher concentrations. Of the sugars tested, maltodextrin and sucrose were the best. Tzeng et al J Control Release 233:11
12 IPV stability: incubation at 37 o C 1 Stability after 28 days of incubation at 37 o C: Type 1 only 1 Stability after 28 days of incubation at 37 o C: Type 1 only No excipient Sorbitol Sorbitol+MSG Sucrose+MSG+MgCl 2 Sucrose Sucrose+MSG Sorbitol+MSG+MgCl 2 Trehalose Trehalose+MSG Trahalose+MSG+MgCl 2 Maltodextrin Maltodextrin+MSG Maltodextrin+MSG+MgCl 2 MSG+MgCl 2 No excipient 27% Sorbitol+MSG+MgCl 2 5% Sorbitol+MSG+MgCl 2 11% Sorbitol+MSG+MgCl 2 27% Sucrose+MSG+MgCl 2 11% Sucrose+MSG+MgCl 2 5% Sucrose+MSG+MgCl 2 11% Trehalose+MSG+MgCl 2 27% Trehalose+MSG+MgCl 2 5% Trehalose+MSG+MgCl 2 27% Maltodextrin+MSG+MgCl 2 5% Maltodextrin+MSG+MgCl 2 1% Gelatin 11% Maltodextrin+MSG+MgCl 2 Sugars on their own did not confer improved stability on IPV during incubation at 37 o C. Sugars performed better when combined with MSG and MgCl 2 and also performed better at higher concentrations. Of the sugars tested, maltodextrin and sucrose were the best. Tzeng et al J Control Release 233:11
13 IPV stability: incubation at 37 o C 1 Stability after 28 days of incubation at 37 o C: Type 1 only 1 Stability after 28 days of incubation at 37 o C: Type 1 only No excipient Sorbitol Sorbitol+MSG Sucrose+MSG+MgCl 2 Sucrose Sucrose+MSG Sorbitol+MSG+MgCl 2 Trehalose Trehalose+MSG Trahalose+MSG+MgCl 2 Maltodextrin Maltodextrin+MSG Maltodextrin+MSG+MgCl 2 MSG+MgCl 2 No excipient 27% Sorbitol+MSG+MgCl 2 5% Sorbitol+MSG+MgCl 2 11% Sorbitol+MSG+MgCl 2 27% Sucrose+MSG+MgCl 2 11% Sucrose+MSG+MgCl 2 5% Sucrose+MSG+MgCl 2 11% Trehalose+MSG+MgCl 2 27% Trehalose+MSG+MgCl 2 5% Trehalose+MSG+MgCl 2 27% Maltodextrin+MSG+MgCl 2 5% Maltodextrin+MSG+MgCl 2 1% Gelatin 11% Maltodextrin+MSG+MgCl 2 Sugars on their own did not confer improved stability on IPV during incubation at 37 o C. Sugars performed better when combined with MSG and MgCl 2 and also performed better at higher concentrations. Of the sugars tested, maltodextrin and sucrose were the best. Tzeng et al J Control Release 233:11
14 IPV stability: incubation at 37 o C 1 Stability after 56 days of incubation at 37 o C Type 1 Type 2 Type No excipient 27% Sorbitol+MSG+MgCl 2 5% Sorbitol+MSG+MgCl 2 27% Sucrose+MSG+MgCl 2 5% Sucrose+MSG+MgCl 2 5% Trehalose+MSG+MgCl 2 27% Trehalose+MSG+MgCl 2 5% Maltodextrin+MSG+MgCl 2 27% Maltodextrin+MSG+MgCl 2 After two months of incubation at 37 o C, IPV formulation with maltodextrin + MSG + MgCl 2 saw good recovery of all three serotypes, with 3-6% recovery of type 1 and 4-7% recovery of types 2 and 3. Tzeng et al J Control Release 233:11
15 Poly(lactic-co-glycolic acid) (PLGA) microparticles for controlled release Biodegradable polyester Hydrolytically cleaved at ester linkages Bulk-degrading Degradation rate depends on lactide-to-glycolide ratio, molecular weight, and formulation parameters Polymer degradation leads to protein release All 3 serotypes of IPV must survive encapsulation, incubation, and release without denaturation IPV must survive drying process
16 IPV stability: Vacuum drying Stability after drying Type 1 Type 2 Type 3 No excipient An aqueous solution of IPV was dried under vacuum for 1 hr at room temperature. IPV alone (without added excipients) was denatured by drying. Excipients and excipient combinations were added to improve stability. Tzeng et al J Control Release 233:11
17 Stability after drying IPV stability: Vacuum drying Type 1 Type 2 Type 3 Gelatin and sugars both showed good results after drying. Sugars generally showed increased protective ability in combination with amino acids (glutamate, MSG) and/or ions (MgCl 2 ). No excipient Gelatin Sorbitol Sorbitol+MSG Sorbitol+MSG+MgCl 2 Sucrose Sucrose+MSG Sucrose+MSG+MgCl 2 Trehalose Trehalose+MSG Maltodextrin+MSG Trahalose+MSG+MgCl 2 Maltodextrin Maltodextrin+MSG+MgCl 2 Tzeng et al J Control Release 233:11
18 Stability after drying IPV stability: Vacuum drying Type 1 Type 2 Type 3 Gelatin and sugars both showed good results after drying. Sugars generally showed increased protective ability in combination with amino acids (glutamate, MSG) and/or ions (MgCl 2 ). No excipient Gelatin Sorbitol Sorbitol+MSG Sorbitol+MSG+MgCl 2 Sucrose Sucrose+MSG Sucrose+MSG+MgCl 2 Trehalose Trehalose+MSG Maltodextrin+MSG Trahalose+MSG+MgCl 2 Maltodextrin Maltodextrin+MSG+MgCl 2 Tzeng et al J Control Release 233:11
19 Stability after drying IPV stability: Vacuum drying Type 1 Type 2 Type 3 Gelatin and sugars both showed good results after drying. Sugars generally showed increased protective ability in combination with amino acids (glutamate, MSG) and/or ions (MgCl 2 ). No excipient Gelatin Sorbitol Sorbitol+MSG Sorbitol+MSG+MgCl 2 Sucrose Sucrose+MSG Sucrose+MSG+MgCl 2 Trehalose Trehalose+MSG Maltodextrin+MSG Trahalose+MSG+MgCl 2 Maltodextrin Maltodextrin+MSG+MgCl 2 Tzeng et al J Control Release 233:11
20 Poly(lactic-co-glycolic acid) (PLGA) microparticles for controlled release Biodegradable polyester Hydrolytically cleaved at ester linkages Bulk-degrading Degradation rate depends on lactide-to-glycolide ratio, molecular weight, and formulation parameters Polymer degradation leads to protein release All 3 serotypes of IPV must survive encapsulation, incubation, and release without denaturation IPV must survive emulsion (sonication)
21 IPV stability: Emulsification (sonication) Stability after sonication Type 1 Type 2 Type 3 Gelatin and showed the best protection of IPV during the sonication step. Sugars and salts generally had minimal effects on the stability during the emulsification step. No excipient Gelatin Sorbitol+MSG+MgCl 2 Sucrose+MSG+MgCl 2 Trahalose+MSG+MgCl 2 Maltodextrin+MSG+MgCl 2 Tzeng et al J Control Release 233:11
22 - Incubation at 37 o C: - Sucrose/MSG/MgCl 2 - Maltodextrin/MSG/MgCl 2 - Drying: - Sorbitol/MSG/MgCl 2 - Maltodextrin/MSG/MgCl 2 - Emulsification: - Gelatin IPV stability: Emulsification (sonication) Gelatin Sorbitol Sorbitol+MSG No excipient Type 1 Type 2 Type 3 Sorbitol+MSG+MgCl 2 Sucrose Sucrose+MSG Sucrose+MSG+MgCl 2 Trehalose Trehalose+MSG Stability after drying No excipient Sorbitol Sorbitol+MSG Trahalose+MSG+MgCl 2 Maltodextrin Maltodextrin+MSG Maltodextrin+MSG+MgCl 2 Stability after 28 days of incubation at 37 o C: Type 1 only Sucrose+MSG+MgCl 2 Sucrose Sucrose+MSG No excipient Sorbitol+MSG+MgCl 2 Trehalose Gelatin Trehalose+MSG Trahalose+MSG+MgCl 2 Maltodextrin Maltodextrin+MSG Maltodextrin+MSG+MgCl 2 MSG+MgCl 2 Stability after sonication Sorbitol+MSG+MgCl 2 Sucrose+MSG+MgCl 2 Trahalose+MSG+MgCl 2 Type 1 Type 2 Type 3 Maltodextrin+MSG+MgCl 2
23 IPV release from PLGA particles Pulsatile release Cumulative release Release Cumulative release Time (days) Time (days) In vitro cumulative release results are plotted as percentages of the human dose (4 DU type 1, 8 DU type 2, 32 DU type 3)
24 IPV release from PLGA particles Gelatin Sucrose, MSG, MgCl 2 Maltodextrin, MSG, MgCl ± 3.6 µ m 1.7 ± 3.4 µ m 11.2 ± 3.4 µ m Cumulative number of doses released per 5 mg particles Type 1 Type 2 Type 3 Gelatin (8%) Time (d) Cumulative number of doses released per 5 mg particles Sucrose (8%), MSG (6.8%), MgCl 2 (6.8%) Type 1 Type 2 Type Time (d) Cumulative number of doses released per 5 mg particles Maltodextrin (8%), MSG (6.8%), MgCl 2 (6.8%) Type 1 Type 2 Type Time (d) - Sugar-based excipients co-encapsulated in PLGA particles promote IPV release in two bursts; however, very little later release is seen for types 1 and 3. Tzeng et al J Control Release 233:11
25 PLGA microspheres: ph PLGA degrades into acidic molecules PLGA degrades by bulk erosion Acid buildup inside microspheres ph of release medium (outside particles) over time suggests acid is also building up inside particles over time ph of release medium PLGA release studies: ph over time 52H 53H Stability after 7 days of incubation at 37 o C Type I Type II Type III time (d) ph
26 PLGA microspheres: Insoluble excipients buffer acidic products Water-soluble bases raise the ph of the IPV environment and cause denaturation Small molecule bases diffuse out of the microparticle faster than the antigen, depleting the basic or buffering component before PLGA degradation is completed Mg(OH) 2 is an insoluble base that can be dispersed in the polymer maxtrix Cumulative number of doses released per 5 mg particles Sucrose (8%), MSG (6.8%), MgCl 2 (6.8%) Type 1 Type 2 Type Time (d) Cumulative number of doses released per 5 mg particles Sucrose (8%), MSG (6.8%), MgCl 2 (6.8%), Mg(OH) 2 (5%) Type 1 Type 2 Type Time (d) Tzeng et al J Control Release 233:11
27 PLGA microspheres: Insoluble excipients buffer acidic products Cationic polymer Eudragit E PO is insoluble in water at neutral ph but soluble at < 3 ph Basic functional groups raise the local ph of PLGA The local basic ph accelerates PLGA degradation, forming acid components that are buffered by the basic Eudragit E
28 PLGA microspheres: cationic polymers as ph-modulating dopants Cumulative number of doses released per 5 mg particles # Human doses released/5 mg Burst Time (d) Maltodextrin, MSG, MgCl % Eudragit E Type 1.5 Type 2 Type Time (d) Type 1 Type 2 Type Cumulative number of doses released per 5 mg particles Type 1.5 Type 2 Type Time (d) # Human doses released/5 mg Burst Time (d) Maltodextrin, MSG, MgCl 2 + 5% Eudragit E Type 1 Type 2 Type Cumulative number of doses released per 5 mg particles Type 1.5 Type 2 Type Time (d) # Human doses released/5 mg Burst Time (d) Maltodextrin, MSG, MgCl 2 + 3% Eudragit E Type 1 Type 2 Type The amount of Eudragit E in the particles controls the spacing of burst release - The formulations shown above release a total of ~2 human doses spread between 2 distinct bursts, mimicking multiple bolus injections Tzeng et al J Control Release 233:11
29 IPV Type 1 Neutralizing Antibodies in Serum 1 Seropositive (%) time (weeks) 1 dose bolus + empty particles All groups: first injection at t= One bolus administration of IPV elicits no detectable neutralizing antibodies against serotype 1.
30 IPV Type 1 Neutralizing Antibodies in Serum 1 Seropositive (%) time (weeks) 1 dose bolus + empty particles 1/2 bolus 2x (, 4 wk) All groups: first injection at t= Boost: t=4 wk Two boluses administered 4 weeks apart are able to elicit neutralizing antibodies against type 1 poliovirus, although the proportion of animals protected against the virus decreased over time.
31 IPV Type 1 Neutralizing Antibodies in Serum 1 Seropositive (%) dose microspheres (F1) 1 dose bolus + empty particles 1/2 bolus 2x (, 4 wk) time (weeks) Boost: t=4 wk All groups: first injection at t= A single injection of IPV-containing microspheres (formulation F1) elicits a strong neutralizing response immediately after injection, without needed a second administration. A single injection of microspheres is equal or superior to two bolus injections and appears to have even longer duration of immunity.
32 IPV Type 2 Neutralizing Antibodies in Serum 1 Seropositive (%) dose 1 dose microspheres (F1) (F1) 1 dose 1 dose bolus bolus + empty + empty particles particles 1/2 1/2 bolus bolus 2x 2x (, (, 4 wk) 4 wk) 1/3 bolus 2x (, 8, 16 wk) time (weeks) Boost: t=4 wk All groups: first injection at t= Immunity against type 2, the most stable of the antigens, is elicited well by the microsphere formulation (red line), matching or exceeding the multiple-bolus controls.
33 IPV Type 3 Neutralizing Antibodies in Serum 1 Seropositive (%) dose 1 dose microspheres (F1) (F1) 1 dose 1 dose bolus bolus + empty + empty particles particles 1/2 1/2 bolus bolus 2x 2x (, (, 4 wk) 4 wk) 1/3 bolus 2x (, 8, 16 wk) time (weeks) Boost: t=4 wk All groups: first injection at t= Interestingly, type 3 stability in the microspheres was poorer in vivo than in the initial in vitro experiments. Further stability studies were conducted to optimize type 3 stability.
34 PLGA microspheres: hydrophilic polycations for improved type 3 stability % human dose per 5 mg microspheres ug/ml polylysine Type 1 Type 2 Type 3 1 ug/ml polylysine IPV Stability 2 ug/ml polylysine.4 ug/ml polylysine ug/ml polylysine Cumulative percent dose released per 5 mg particles Maltodextrin, MSG, MgCl 2 + 3% b-pei(1.8k) +.8% Poly(lysine) Type 1 Type Time (d) # Human doses released/5 mg Burst Time (d) Type 1 Type 2 Type An optimized concentration of poly(l-lysine) (PLL) improves IPV stability, particularly for types 1 and 3. - Higher overall release and higher late type 3 release are observed from microspheres that co-encapsulate polycations, such as PLL and low MW polyethylenimine (PEI).
35 IPV in vivo experiment (next iteration): Neutralizing antibodies (2 weeks) 2 week titers - type 3 2 week titers - type Log 2 (Titer) 8 6 Log 2 (Titer) /3 dose bolus 3x (, 8, 16 wk) 1/2 bolus 2x (, 4 wk) 1 dose microspheres F5 1 dose bolus 1 dose bolus + empty particles 1 dose microspheres F1 2 1/2 bolus 2x (, 4 wk) 1/3 dose bolus 3x (, 8, 16 wk) 1 dose microspheres F5 1 dose bolus 1 dose bolus + empty particles 1 dose microspheres F1 Type 1: F1 microspheres (red) elicited neutralizing antibodies within 2 weeks, while none of the bolus controls did. The new formulation F5 (purple) is superior to F1 at the early time point. Type 3: The new formulation F5 (purple) is superior to the previous formulation F1 and, importantly, superior to the bolus controls. Importantly, the low dose of F5, in which the dosage was calculated by theoretical loading (i.e. assuming no loss of IPV doses due to processing or stability) is still superior to all controls and previous formulations.
36 Summary Excipients can stabilize IPV against thermal and physical stresses over time IPV co-encapsulated with stabilizers and ph-modulators can be released in a pulsatile manner from PLGA particles Encapsulated IPV elicits a more potent neutralizing antibody response in vivo than free IPV injected as a bolus Future Directions Expand pulsatile or continuous release platform to other vaccines Sabin IPV (sipv), experimental HIV vaccines, etc. Investigate the effect of types of release kinetics on immune response Increase the number of pulses that are released in vivo Pulsatile release of vaccines from core-shell particles Poster #23
37 Acknowledgements MIT: Langer lab Robert Langer, ScD Ana Jaklenec, PhD Bill and Melinda Gates Foundation Rohiverth Guarecuco Jennifer Lu David Yang James Sugarman Allison Linehan Sviatlana Rose Thanh Nguyen, PhD Matthias Oberli, PhD Kevin McHugh, PhD Aaron Anselmo, PhD Adam Behrens, PhD Shiran Ferber, PhD Corey Bishop, PhD James Norman, PhD
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