Role of particle size, shape, and stiffness in design of intravascular drug delivery systems: Insights from computations, experiments, and nature

Wiley Interdisciplinary Reviews: Nanomedicine and Nanobiotechnology

Volumn 8, Issue 2, 2016, Pages 255-270

  Sen Gupta, Anirban ^a  

^a Case Western Reserve University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOCOMPATIBILITY; BIOLOGICAL MATERIALS; FABRICATION; PARTICLE SIZE; STIFFNESS; SURFACE CHEMISTRY;

CELLULAR COMPONENTS; CLINICAL TRANSLATION; COMPUTATIONAL MODEL; DRUG CARRIER SYSTEMS; DRUG DELIVERY SYSTEM; INTERDISCIPLINARY RESEARCH; MICRO-FLUIDIC DEVICES; PARTICULATE DRUG DELIVERY SYSTEMS;

DESIGN;

BIOMATERIAL;

BLOOD COMPONENT; CELL ADHESION; CIRCULATION; DRUG DELIVERY SYSTEM; DRUG DESIGN; DRUG PACKAGING; INTERNALIZATION; INTRAVASCULAR DRUG ADMINISTRATION; MACROMOLECULE; PARTICLE SIZE; PHYSICAL CHEMISTRY; PRIORITY JOURNAL; REVIEW; SHEAR FLOW; SURFACE PROPERTY; BLOOD VESSEL; COMPUTER SIMULATION; HUMAN; MECHANICS; PHYSIOLOGY; PROCEDURES;

BLOOD VESSELS; COMPUTER SIMULATION; DRUG DELIVERY SYSTEMS; HUMANS; MECHANICAL PHENOMENA; PARTICLE SIZE;

EID: 84959208434     PISSN: 19395116     EISSN: 19390041     Source Type: Journal    
DOI: 10.1002/wnan.1362     Document Type: Review

References (83)

1. Maeda H, Wu J, Sawa T, Matsumura Y, Hori K. Tumor vascular permeability and the EPR effect in macromolecular therapeutics: a review. J Control Release 2000, 65:271-284.
2. Fang J, Nakamura H, Maeda H. The EPR effect: unique features of tumor blood vessels for drug delivery, factors involved, and limitations and augmentation of the effect. Adv Drug Deliv Rev 2011, 63:136-151.
3. Hobbs SK, Monsky WL, Yuan F, Roberts WG, Griffith L, Torchilin VP, Jain RK. Regulation of transport pathways in tumor vessels: role of tumor type and microenvironment. Proc Natl Acad Sci USA 1998, 95:4607-4612.
4. Goldsmith HL, Marlow J. Flow behaviour of erythrocytes. I. Rotation and deformation in dilute suspensions. Proc R Soc Lond B 1972, 182:351-384.
5. Puig-de-Morales-Marinkovic M, Turner KT, Butler JP, Fredberg JF, Suresh S. Viscoelasticity of the human red blood cell. Am J Physiol Cell Physiol 2007, 293:C597-C605.
6. Canham P, Burton A. Distribution of size and shape in population of normal human red cells. Circ Res 1968, 22:405-416.
7. Frojmovic MM, Milton JG. Human platelet size, shape and related functions in human health and disease. Physiol Rev 1982, 62:185-261.
8. Italiano JE Jr, Bergmeier W, Tiwari S, Falet H, Hartwig JH, Hoffmeister KM, André P, Wagner DD, Shivdasani RA. Mechanisms and implications of platelet discoid shape. Blood 2003, 101:4789-4796.
9. Radmacher M, Fritz M, Kacher CM, Cleveland JP, Hansma PK. Measuring the viscoelastic properties of human platelets with the atomic force microscope. Biophys J 1996, 70:556-567.
10. Schmid-Schonbein GW, Sung K-LP, Tozeren H, Skalak R, Chien S. Passive mechanical properties of human leukocytes. Biophys J 1981, 36:243-256.
11. Patil VRS, Campbell CJ, Yun YH, Slack SM, Goetz DJ. Particle diameter influences adhesion under flow. Biophys J 2001, 80:1733-1743.
12. Decuzzi P, Gentile F, Granaldi A, Curcio A, Causa F, Indolfi C, Netti P, Ferrari M. Flow chamber analysis of size effects in the adhesion of spherical particles. Int J Nanomed 2007, 2:689-696.
13. Gentile F, Curcio A, Indolfi C, Ferrari M, Decuzzi P. The margination propensity of spherical particles for vascular targeting in the microcirculation. J Nanobiotechnol. 2008, 6:9.
14. Lee S-Y, Ferrari M, Decuzzi P. Shaping nano-/micro-particles for enhanced vascular interaction in laminar flows. Nanotechnology 2009, 20:495101 (11pp).
15. Decuzzi P, Lee S, Bhushan B, Ferrari M. A theoretical model for the margination of particles within blood vessels. Ann Biomed Eng 2005, 33:179-190.
16. Toy R, Hayden E, Shoup C, Baskaran H, Karathanasis E. The effects of particle size, density and shape on margination of nanoparticles in microcirculation. Nanotechnology 2011, 22:115101.
17. Charoenphol P, Mocherla S, Bouisc D, Namdeeb K, Pinsky DJ, Eniola-Adefeso O. Targeting therapeutics to the vascular wall in atherosclerosis-carrier size matters. Atherosclerosis 2011, 217:364-370.
18. Charoenphol P, Huang RB, Eniola-Adefeso O. Potential role of size and hemodynamics in the efficacy of vascular-targeted spherical drug carriers. Biomaterials 2010, 31:1392-1402.
19. Charoenphol P, Onyskiw PJ, Carrasco-Teja M, Eniola-Adefeso O. Particle-cell dynamics in human blood flow: implications for vascular-targeted drug delivery. J Biomech 2012, 45:2822-2828.
20. Conner SD, Schmid SL. Regulated portals of entry into the cell. Nature 2003, 422:37-44.
21. Best JP, Yan Y, Caruso F. The role of particle geometry and mechanics in the biological domain. Adv Healthc Mater 2012, 1:35-47.
22. Wang J, Byrne JD, Napier ME, DeSimone JM. More effective nanomedicines through particle design. Small 2011, 7:1919-1931.
23. Foged C, Brodin B, Frokajaer S, Sundblad A. Particle size and surface charge affect particle uptake by human dendritic cells in an in vitro model. Int J Pharm 2005, 298:315-322.
24. Muro S, Garnacho C, Champion JA, Leferovich J, Gajewski C, Schuchman EH, Mitragotri S, Muzykantov V. Control of endothelial targeting and intracellular delivery of therapeutic enzymes by modulating the size and shape of ICAM-1-targeted carriers. Mol Ther 2008, 16:1450-1458.
25. Gratton SEA, Ropp PA, Pohlhaus PD, Luft JC, Madden VJ, Napier ME, DeSimone J. The effect of particle design on cellular internalization pathways. Proc Natl Acad Sci USA 2008, 105:11613-11618.
26. Gref R, Domb A, Quellec P, Blunk T, Müller RH, Verbavatz JM, Langer R. The controlled intravenous delivery of drugs using PEG-coated sterically stabilized nanospheres. Adv Drug Deliv Rev 1995, 16:215-233.
27. Owens DE III, Peppas NA. Opsonization, biodistribution, and pharmacokinetics of polymeric nanoparticles. Int J Pharm 2006, 307:93-102.
28. Kulkarni SA, Feng S-S. Effects of particle size and surface modification on cellular uptake and biodistribution of polymeric nanoparticles for drug delivery. Pharm Res 2013, 30:2512-2522.
29. Champion JA, Walker A, Mitragotri S. Role of particle size in phagocytosis of polymeric microspheres. Pharm Res 2008, 25:1815-1821.
30. Pacheco P, White D, Sulchek T. Effects of microparticle size and Fc density on macrophage phagocytosis. PLoS ONE 2013, 8:e60989. doi:10.1371/journal.pone.0060989.
31. Decuzzi P, Ferrari M. The adhesive strength of non-spherical particles mediated by specific interactions. Biomaterials 2006, 27:5307-5314.
32. Gentile F, Chiappini C, Fine D, Bhavane RC, Peluccio MS, Cheng MM-C, Liu X, Ferrari M, Decuzzi P. The effect of shape on the margination dynamics of non-neutrally buoyant particles in two-dimensional shear flows. J Biomech 2008, 41:2312-2318.
33. Gavze E, Shapiro M. Motion of inertial spheroidal particles in shear flow near a solid wall with special application to aerosol transport in microgravity. J Fluid Mech 1998, 371:59-79.
34. Shah S, Liu Y, Hu W, Gao J. Modeling particle shape-dependent dynamics in nanomedicine. J Nanosci Nanotechnol 2011, 11:919-928.
35. Geng Y, Dalhaimer P, Cai S, Tsai R, Tewari M, Minko T, Discher DE. Shape effects of filaments versus spherical particles in flow and drug delivery. Nat Nanotechnol 2007, 2:249-255.
36. Tao L, Hu W, Liu Y, Huang G, Sumer BD, Gao J. Shape-specific polymeric nanomedicine: emerging opportunities and challenges. Exp Biol Med 2011, 236:20-29.
37. Thompson AJ, Mastra EM, Eniola-Adefeso O. The margination propensity of ellipsoidal micro/nanoparticles to the endothelium in human blood flow. Biomaterials 2013, 34:5863-5871.
38. Holme MN, Fedotenko IA, Abegg D, Althaus J, Babel L, Favarger F, Reiter R, Tanasescu R, Zaffalon P-L, Ziegler A, et al. Shear-stress sensitive lenticular vesicles for targeted drug delivery. Nat Nanotechnol 2012, 7:536-543.
39. Heslinga MJ, Mastria EM, Eniola-Adefeso O. Fabrication of biodegradable spheroidal microparticles for drug delivery applications. J Control Release 2009, 138:235-242.
40. Heslinga MJ, Willis GM, SobcZynski DJ, Thompson AJ, Eniola-Adefeso O. One-step fabrication of agent-loaded biodegradable microspheroids for drug delivery and imaging applications. Colloids Surf B Biointerfaces 2014, 116:55-62.
41. Park J-H, Maltzahn G, Zhang L, Schwartz MP, Ruoslahti E, Bhatia SN, Sailor MJ. Magnetic iron oxide nanoworms for tumor targeting and imaging. Adv Mater 2008, 20:1630-1635.
42. Peiris PM, Toy R, Abramowski A, Vicente P, Tucci S, Bauer L, Mayer A, Tam M, Doolittle E, Pansky J, et al. Treatment of cancer micrometastasis using a multicomponent chain-like nanoparticle. J Control Release 2014, 173:51-58.
43. Yang Z, Huck WTS, Clark SM, Tajbakhsh AR, Ternet Jev EM. Shape-memory nanoparticles from inherently non-spherical polymer colloids. Nat Mater 2005, 4:486-490.
44. Chou SY, Krauss PR, Renstrom PJ. Nanoimprint lithography. J Vac Sci Technol B 1996, 14:4129-4133.
45. Colburn M, Johnson SC, Stewart MD, Damle S, Bailey TC, Choi B, Wedlake M, Michaelson TB, Sreenivasan SV, Ekerdt JG, et al. Step and flash imprint lithography: a new approach to high-resolution patterning. Proc SPIE 1999, 3676:379-389.
46. Xia Y, Whitesides GM. Soft lithography. Angew Chem Int Ed 1998, 37:550-575.
47. Dendukuri D, Pregibon DC, Collins J, Hatton TA, Doyle PS. Continuous-flow lithography for high-throughput microparticle synthesis. Nat Mater 2006, 5:365-369.
48. Rolland JP, Maynor BW, Euliss LE, Exner AE, Denison GM, DeSimone JM. Direct fabrication and harvesting of monodisperse, shape-specific nanobiomaterials. J Am Chem Soc 2005, 127:10096-10100.
49. Xu J, Wong DHC, Byrne JD, Chen K, Bowerman C, DeSimone JM. Future of the particle replication in nonwetting templates (PRINT) technology. Angew Chem Int Ed 2013, 52:6580-6589.
50. Champion JA, Katare YK, Mitragotri S. Making polymeric micro and nanoparticles of complex shapes. Proc Natl Acad Sci USA 2007, 104:11901-11904.
51. Champion JA, Katare YK, Mitragotri S. Particle shape: a new design parameter for micro- and nanoscale drug delivery carriers. J Control Release 2007, 121:3-9.
52. Glangchai LC, 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.
53. Caldorera-Moore M, Guimard N, Shi L, Roy K. Designer nanoparticles: incorporating size, shape, and triggered release into nanoscale drug carriers. Expert Opin Drug Deliv 2010, 7:479-495.
54. Tao L, Crouch A, Yoon F, Lee BK, Guthi JS, Kim J, Gao J, Hu W. Surface energy induced patterning of organic and inorganic materials on heterogeneous Si surfaces. J Vac Sci Technol B 2007, 25:1993-1997.
55. Tao L, Zhao XM, Gao JM, Hu W. Lithographically defined uniform worm-shaped polymeric nanoparticles. Nanotechnology 2010, 21:095301.
56. Wang Y, Merkel TJ, Chen K, Fromen CA, Betts DE, DeSimone JM. Generation of a library of particles having controlled sizes and shapes via the mechanical elongation of master template. Langmuir 2011, 27:524-528.
57. Merkel TJ, Jones SW, Herlihy KP, Kersey FR, Shields AR, Napier M, Luft JC, Wu H, Zamboni WC, Wang AZ, et al. Using mechanobiological mimicry of red blood cells to extend circulation times of hydrogel microparticles. Proc Natl Acad Sci USA 2001, 108:586-591.
58. Doshi N, Zahr AS, Bhasakar S, Lahann J, Mitragotri S. Red blood cell-mimicking synthetic biomaterial particles. Proc Natl Acad Sci USA 2009, 106:21495-21499.
59. Doshi N, Prabhakarpandian B, Rea-Ramsey A, Pant K, Sundaram S, Mitragotri S. Flow and adhesion of drug carriers in blood vessels depend on their shape: a study using model synthetic microvascular networks. J Control Release 2010, 146:196-200.
60. Doshi N, Swiston AJ, Gilbert JB, Alcaraz ML, Cohen RE, Rubner MF, Mitragotri S. Cell-based drug delivery devices using phagocytosis-resistant backpacks. Adv Mater 2011, 23:H105-H109.
61. Doshi N, Orje J, Molins B, Smith J, Mitragotri S, Ruggeri Z. Platelet mimetic particles for targeting thrombi in flowing blood. Adv Mater 2012, 24:3864-3869.
62. Kolhar P, Anselmo A, Gupta V, Prabhakarpandian B, Pant K, Ruoslahti R, Mitragotri S. Using shape effects to target nanoparticles to lung and brain endothelium. Proc Natl Acad Sci USA 2013, 110:10753-10758.
63. Barua S, Yoo J-W, Kolhar P, Wakankar A, Gokarn Y, Mitragotri S. Particle shape enhances avidity and specificity of antibodies. Proc Natl Acad Sci USA 2013, 2013:3270-3275.
64. Anselmo AC, Modery-Pawlowski CL, Menegatti S, Kumar S, Vogus DR, Tian LL, Chen M, Squires TM, Sen Gupta A, Mitragotri S. Platelet-like nanoparticles: mimicking shape, flexibility, and surface biology of platelets to target vascular injuries. ACS Nano 2014, 8:11243-11253.
65. Toksvang LN, Berg RMG. Using a classic paper by Robin Fåhraeus and Torsten Lindqvist to teach basic hemorheology. Adv Physiol Educ 2013, 37:129-133.
66. Alapan Y, Little JA, Gurkan UA. Heterogeneous red blood cell adhesion and deformability in sickle cell disease. Sci Rep 2014, 4:7173.
67. Freund JB. Leukocyte margination in a model microvessel. Phys Fluids 2007, 19:023301.
68. Kumar A, Graham MD. Segregation by membrane rigidity in flowing binary suspensions of elastic capsules. Phys Rev E Stat Nonlin Soft Matter Phys 2011, 84:066316.
69. Kumar A, Graham MD. Margination and segregation in confined flows of blood and other multicomponent suspensions. Soft Matter 2012, 8:10536-10548.
70. Reasor DA Jr, Mehrabadi M, Ku DN, Aidun CK. Determination of critical parameters in platelet margination. Ann Biomed Eng 2013, 41:238-249.
71. AlMomani T, Udaykumar HS, Marshall JS, Chandran KB. Micro-scale dynamic simulation of erythrocyte-platelet interaction in blood flow. Ann Biomed Eng 2008, 36:905-920.
72. Wang W, Diacovo TG, Chen J, Freund JB, King MR. Simulation of platelet, thrombus and erythrocyte hydrodynamic interactions in a 3D arteriole with in vivo comparison. PLoS ONE 2013, 8:e76949.
73. Müller K, Fedosov DA, Gompper G. Margination of micro- and nano-particles in blood flow and its effect on drug delivery. Sci Rep 2014, 4:4871.
74. Tokarev AA, Butylin AA, Ataullakhanov FI. Platelet adhesion from shear blood flow is controlled by near-wall rebounding collisions with erythrocytes. Biophys J 2011, 100:799-808.
75. Zhao H, Shaqfeh ESG. Shear-induced platelet margination in a microchannel. Phys Rev 2011, 83:061924.
76. Murciano J-C, Medinilla S, Eslin D, Atochina E, Cines DB, Muzykantov VR. Prophylactic fibrinolysis through selective dissolution of nascent clots by tPA-carrying erythrocytes. Nat Biotechnol 2003, 21:891-896.
77. Modery-Pawlowski CL, Tian LL, Pan V, McCrae KR, Mitragotri S, Sen Gupta A. Approaches to synthetic platelet analogs. Biomaterials 2013, 34:526-541.
78. Modery-Pawlowski CL, Tian LL, Pan V, Sen Gupta A. Synthetic approaches to RBC mimicry and oxygen carrier systems. Biomacromolecules 2013, 14:939-948.
79. Shukla S, Eber FJ, Nagarajan AS, DiFranco NA, Schmidt N, Wen AM, Eiben S, Twyman RM, Wege C, Steinmetz NF. The impact of aspect ratio on the biodistribution and tumor homing of rigid soft-matter nanorods. Adv Healthc Mater 2015, 4:874-882. doi:10.1002/adhm.201400641.
80. Howard N, Zern BJ, Anselmo AC, Shuvaev VV, Mitragotri S, Muzykantov V. Vascular targeting of nanocarriers: perplexing aspects of the seeming straightforward paradigm. ACS Nano 2014, 8:4100-4132.
81. Vahidkhah K, Bagchi P. Microparticle shape effects on margination, near-wall dynamics and adhesion in a three-dimensional simulation of red blood cell suspension. Soft Matter 2015, 11:2097-2109.
82. Serda RE, Godin B, Blanco E, Chiappini C, Ferrari M. Multi-stage delivery nano-particle systems for therapeutic applications. Biochim Biophys Acta 1810, 2011:317-329.
83. Korin N, Kanapathipillai M, Matthews BD, Crescente M, Brill A, Mammoto T, Ghosh K, Jurek S, Bencherif SA, Bhatta D, et al. Shear-activated nanotherapeutics for drug targeting to obstructed blood vessels. Science 2012, 337:738-742.