Design and Characterization of Fibrin-Based Acoustically Responsive Scaffolds for Tissue Engineering Applications

Ultrasound in Medicine and Biology

Volumn 42, Issue 1, 2016, Pages 257-271

  Moncion, Alexander ^a,b   Arlotta, Keith J ^b   Kripfgans, Oliver D ^a,b   Fowlkes, J Brian ^a,b   Carson, Paul L ^a,b   Putnam, Andrew J ^a   Franceschi, Renny T ^a,c   Fabiilli, Mario L ^a,b  

^a UNIVERSITY OF MICHIGAN   (United States)

^b UNIVERSITY OF MICHIGAN HEALTH SYSTEM   (United States)

^c UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

Acoustic droplet vaporization; Controlled release; Emulsion; Fibrin; Inertial cavitation; Perfluorocarbon; Spatiotemporal drug delivery; Ultrasound

Indexed keywords

CAVITATION; CONTROLLED DRUG DELIVERY; DROPS; EMULSIFICATION; EMULSIONS; HYDROGELS; TISSUE; TISSUE ENGINEERING; TISSUE REGENERATION; ULTRASONICS; VAPORIZATION;

ACOUSTIC DROPLET VAPORIZATION; CONTROLLED RELEASE; FIBRIN; INERTIAL CAVITATION; PERFLUOROCARBONS;

SCAFFOLDS (BIOLOGY);

FIBRIN; PERFLEXANE; PERFLUOROPENTANE; EMULSION; FLUOROCARBON;

ACOUSTIC DROPLET VAPORIZATION; ACOUSTICALLY RESPONSIVE SCAFFOLD; ACOUSTICS; ARTICLE; CELL ENCAPSULATION; CELL VIABILITY; CONTROLLED STUDY; EMULSION; EQUIPMENT DESIGN; PRESSURE; SPATIOTEMPORAL ANALYSIS; TISSUE ENGINEERING; TISSUE SCAFFOLD; ULTRASOUND; ULTRASOUND SCANNER; ULTRASOUND TRANSDUCER; VAPORIZATION; CELL SURVIVAL; CHEMISTRY; POLARIZATION MICROSCOPY; PROCEDURES; VOLATILIZATION;

ACOUSTICS; CELL SURVIVAL; EMULSIONS; FIBRIN; FLUOROCARBONS; MICROSCOPY, POLARIZATION; PRESSURE; TISSUE ENGINEERING; TISSUE SCAFFOLDS; ULTRASONICS; VOLATILIZATION;

EID: 85009355210     PISSN: 03015629     EISSN: 1879291X     Source Type: Journal    
DOI: 10.1016/j.ultrasmedbio.2015.08.018     Document Type: Article

References (72)

1. Ammi, A.Y., Cleveland, R.O., Mamou, J., Wang, G.I., Bridal, S.L., O'Brien, W.D., Ultrasonic contrast agent shell rupture detected by inertial cavitation and rebound signals. IEEE Trans Ultrason Ferroelectr Freq Control 53 (2006), 126–136.
2. Apfel, R.E., Possibility of microcavitation from diagnostic ultrasound. IEEE Trans Ultrason Ferroelectr Freq Control 33 (1986), 139–142.
3. Apfel, R.E., Holland, C.K., Gauging the likelihood of cavitation from short-pulse, low-duty cycle diagnostic ultrasound. Ultrasound Med Biol 17 (1991), 179–185.
4. Atchley, A.A., Frizzell, L.A., Apfel, R.E., Holland, C.K., Madanshetty, S., Roy, R.A., Thresholds for cavitation produced in water by pulsed ultrasound. Ultrasonics 26 (1988), 280–285.
5. Barthes, J., Ozcelik, H., Hindie, M., Ndreu-Halili, A., Hasan, A., Vrana, N.E., Cell microenvironment engineering and monitoring for tissue engineering and regenerative medicine: The recent advances. Biomed Res Int, 3, 2014, 921905.
6. Bos, P.K., van Osch, G.J.V.M., Frenz, D.A., Verhaar, J.A.N., Verwoerd-Verhoef, H.L., Growth factor expression in cartilage wound healing: Temporal and spatial immunolocalization in a rabbit auricular cartilage wound model. Osteoarthritis Cartilage 9 (2001), 382–389.
7. Brennen, C.E., Fission of collapsing cavitation bubbles. J Fluid Mech 472 (2002), 153–166.
8. Chen, W.S., Matula, T.J., Crum, L.A., The disappearance of ultrasound contrast bubbles: Observations of bubble dissolution and cavitation nucleation. Ultrasound Med Biol 28 (2002), 793–803.
9. Chen, W.S., Matula, T.J., Brayman, A.A., Crum, L.A., A comparison of the fragmentation thresholds and inertial cavitation doses of different ultrasound contrast agents. J Acoust Soc Am 113 (2003), 643–651.
10. Dayton, P.A., Morgan, K.E., Klibanov, A.L., Brandenburger, G.H., Ferrara, K.W., Optical and acoustical observations of the effects of ultrasound on contrast agents. IEEE Trans Ultrason Ferroelectr Freq Control 46 (1999), 220–232.
11. Dehghani, F., Annabi, N., Engineering porous scaffolds using gas-based techniques. Curr Opin Biotechnol 22 (2011), 661–666.
12. Dias, A.M.A., Freire, M., Coutinho, J.A.P., Marrucho, I.M., Solubility of oxygen in liquid perfluorocarbons. Fluid Phase Equilibria 222 (2004), 325–330.
13. 19F-MRI. Pharm Res 27 (2010), 1–16.
14. Epstein, P.S., Plesset, M.S., On the stability of gas bubbles in liquid-gas solutions. J Chem Phys 18 (1950), 1505–1509.
15. Epstein-Barash, H., Orbey, G., Polat, B.E., Ewoldt, R.H., Feshitan, J., Langer, R., Borden, M.A., Kohane, D.S., A microcomposite hydrogel for repeated on-demand ultrasound-triggered drug delivery. Biomaterials 31 (2010), 5208–5217.
16. Fabiilli, M.L., Haworth, K.J., Fakhri, N.H., Kripfgans, O.D., Carson, P.L., Fowlkes, J.B., The role of inertial cavitation in acoustic droplet vaporization. IEEE Trans Ultrason Ferroelectr Freq Control 56 (2009), 1006–1017.
17. Fabiilli, M.L., Haworth, K.J., Sebastian, I.E., Kripfgans, O.D., Carson, P.L., Fowlkes, J.B., Delivery of chlorambucil using an acoustically-triggered perfluoropentane emulsion. Ultrasound Med Biol 36 (2010), 1364–1375.
18. Fabiilli, M.L., Lee, J.A., Kripfgans, O.D., Carson, P.L., Fowlkes, J.B., Delivery of water-soluble drugs using acoustically triggered perfluorocarbon double emulsions. Pharm Res 27 (2010), 2753–2765.
19. Fabiilli, M.L., Wilson, C.G., Padilla, F., Martin-Saavedra, F.M., Fowlkes, J.B., Franceschi, R.T., Acoustic droplet–hydrogel composites for spatial and temporal control of growth factor delivery and scaffold stiffness. Acta Biomater 9 (2013), 7399–7409.
20. Faithfull, N.S., Oxygen delivery from fluorocarbon emulsions: Aspects of convective and diffusive transport. Biomater Artif Cells Immobilization Biotechnol 20 (1992), 797–804.
21. Ferrara, K.W., Pollard, R., Borden, M.A., Ultrasound microbubble contrast agents: Fundamentals and application to gene and drug delivery. Annu Rev Biomed Eng 9 (2007), 425–447.
22. Flynn, H.G., Church, C.C., A mechanism for the generation of cavitation maxima by pulsed ultrasound. J Acoust Soc Am 76 (1984), 505–512.
23. Fowlkes, J.B., Crum, L.A., Cavitation threshold measurements for microsecond length pulses of ultrasound. J Acoust Soc Am 83 (1988), 2190–2201.
24. Frimpong, R.A., Fraser, S., Hilt, J.Z., Synthesis and temperature response analysis of magnetic-hydrogel nanocomposites. J Biomed Mater Res Pt A 80A (2007), 1–6.
25. Fujie, T., Mori, Y., Ito, S., Nishizawa, M., Bae, H., Nagai, N., Onami, H., Abe, T., Khademhosseini, A., Kaji, H., Micropatterned polymeric nanosheets for local delivery of an engineered epithelial monolayer. Adv Mater 26 (2014), 1699–1705.
26. Giesecke, T., Hynynen, K., Ultrasound-mediated cavitation thresholds of liquid perfluorocarbon droplets in vitro. Ultrasound Med Biol 29 (2003), 1359–1365.
27. Hallow, D.M., Mahajan, A.D., McCutchen, T.E., Prausnitz, M.R., Measurement and correlation of acoustic cavitation with cellular bioeffects. Ultrasound Med Biol 32 (2006), 1111–1122.
28. Holland, C.K., Apfel, R.E., An improved theory for the prediction of microcavitation thresholds. IEEE Trans Ultrason Ferroelectr Freq Control 36 (1989), 204–208.
29. Huebsch, N., Kearney, C.J., Zhao, X.H., Kim, J., Cezar, C.A., Suo, Z.G., Mooney, D.J., Ultrasound-triggered disruption and self-healing of reversibly cross-linked hydrogels for drug delivery and enhanced chemotherapy. Proc Natl Acad Sci U S A 111 (2014), 9762–9767.
30. Hwang, J.H., Tu, J., Brayman, A.A., Matula, T.J., Crum, L.A., Correlation between inertial cavitation dose and endothelial cell damage in vivo. Ultrasound Med Biol 32 (2006), 1611–1619.
31. Javadi, M., Pitt, W.G., Tracy, C.M., Barrow, J.R., Willardson, B.M., Hartley, J.M., Tsosie, N.H., Ultrasonic gene and drug delivery using eLiposomes. J Control Release 167 (2013), 92–100.
32. Johnson, J.L.H., Dolezal, M.C., Kerschen, A., Matsunaga, T.O., Unger, E.C., In vitro comparison of dodecafluoropentane (DDFP), perfluorodecalin (PFD), and perfluoroctylbromide (PFOB) in the facilitation of oxygen exchange. Artif Cells Blood Substitutes Biotechnol 37 (2009), 156–162.
33. Kandadai, M.A., Mohan, P., Lin, G., Butterfield, A., Skliar, M., Magda, J.J., Comparison of surfactants used to prepare aqueous perfluoropentane emulsions for pharmaceutical applications. Langmuir 26 (2010), 4655–4660.
34. Kawabata, K.I., Sugita, N., Yoshikawa, H., Azuma, T., Umemura, S.I., Nanoparticles with multiple perfluorocarbons for controllable ultrasonically induced phase shifting. Jpn J Appl Phys 44 (2005), 4548–4552.
35. Kniazeva, E., Kachgal, S., Putnam, A.J., Effects of extracellular matrix density and mesenchymal stem cells on neovascularization in vivo. Tissue Eng Pt A 17 (2011), 905–914.
36. Kripfgans, O.D., Fowlkes, J.B., Miller, D.L., Eldevik, O.P., Carson, P.L., Acoustic droplet vaporization for therapeutic and diagnostic applications. Ultrasound Med Biol 26 (2000), 1177–1189.
37. Kripfgans, O.D., Fowlkes, J.B., Woydt, M., Eldevik, O.P., Carson, P.L., In vivo droplet vaporization for occlusion therapy and phase aberration correction. IEEE Trans Ultrason Ferroelectr Freq Control 49 (2002), 726–738.
38. Kripfgans, O.D., Fabiilli, M.L., Carson, P.L., Fowlkes, J.B., On the acoustic vaporization of micrometer-sized droplets. J Acoust Soc Am 116 (2004), 272–281.
39. Kulkarni, R., Biswanath, S., Electrically responsive smart hydrogels in drug delivery: A review. J Appl Biomater Biomech 5 (2007), 125–139.
40. Lavigne, M.D., Pennadam, S.S., Ellis, J., Yates, L.L., Alexander, C., Gorecki, D.C., Enhanced gene expression through temperature profile-induced variations in molecular architecture of thermoresponsive polymer vectors. J Gene Med 9 (2007), 44–54.
41. Lima, E.G., Durney, K.M., Sirsi, S.R., Nover, A.B., Ateshian, G.A., Borden, M.A., Hung, C.T., Microbubbles as biocompatible porogens for hydrogel scaffolds. Acta Biomater 8 (2012), 4334–4341.
42. Madanshetty, S.I., Apfel, R.E., Acoustic microcavitation: Enhancement and applications. J Acoust Soc Am 90 (1991), 1508–1514.
43. Marchioni, C., Riccardi, E., Spinelli, S., dell'Unto, F., Grimaldi, P., Bedini, A., Giliberti, C., Giuliani, L., Palomba, R., Castellano, A.C., Structural changes induced in proteins by therapeutic ultrasounds. Ultrasonics 49 (2009), 569–576.
44. Martz, T.D., Sheeran, P.S., Bardin, D., Lee, A.P., Dayton, P.A., Precision manufacture of phase-change perfluorocarbon droplets using microfluidics. Ultrasound Med Biol 37 (2011), 1952–1957.
45. Matsusaki, M., Akashi, M., Novel functional biodegradable polymer IV: pH-sensitive controlled release of fibroblast growth factor-2 from a poly(gamma-glutamic acid)–sulfonate matrix for tissue engineering. Biomacromolecules 6 (2005), 3351–3356.
46. Meijering, B.D.M., Henning, R.H., Van Gilst, W.H., Gavrilovic, I., Van Wamel, A., Deelman, L.E., Optimization of ultrasound and microbubbles targeted gene delivery to cultured primary endothelial cells. J Drug Target 15 (2007), 664–671.
47. Metallo, C.M., Mohr, J.C., Detzel, C.J., de Pablo, J.J., Van Wie, B.J., Palecek, S.P., Engineering the stem cell microenvironment. Biotechnol Prog 23 (2007), 18–23.
48. Nair, A., Thevenot, P., Dey, J., Shen, J.H., Sun, M.W., Yang, J., Tang, L.P., Novel polymeric scaffolds using protein microbubbles as porogen and growth factor carriers. Tissue Eng Pt C 16 (2010), 23–32.
49. Pishchalnikov, Y.A., McAteer, J.A., Pishchalnikova, I.V., Williams, J.C., Bailey, M.R., Sapozhnikov, O.A., Bubble proliferation in shock wave lithotripsy occurs during inertial collapse. Enflo, B.O., Hedberg, C.M., Kari, L., (eds.) Nonlinear acoustics fundamentals and applications, 2008, American Institute of Physics, College Park, MD, 460–463.
50. Rahim, A., Taylor, S.L., Bush, N.L., Ter Haar, G.R., Bamber, J.C., Porter, C.D., Physical parameters affecting ultrasound/microbubble-mediated gene delivery efficiency in vitro. Ultrasound Med Biol 32 (2006), 1269–1279.
51. Rahim, A.A., Taylor, S.L., Bush, N.L., ter Haar, G.R., Bamber, J.C., Porter, C.D., Spatial and acoustic pressure dependence of microbubble-mediated gene delivery targeted using focused ultrasound. J Gene Med 8 (2006), 1347–1357.
52. Rapoport, N.Y., Kennedy, A.M., Shea, J.E., Scaife, C.L., Nam, K.H., Controlled and targeted tumor chemotherapy by ultrasound-activated nanoemulsions/microbubbles. J Control Release 138 (2009), 268–276.
53. Rapoport, N., Nam, K.H., Gupta, R., Gao, Z.G., Mohan, P., Payne, A., Todd, N., Liu, X., Kim, T., Shea, J., Scaife, C., Parker, D.L., Jeong, E.K., Kennedy, A.M., Ultrasound-mediated tumor imaging and nanotherapy using drug loaded, block copolymer stabilized perfluorocarbon nanoemulsions. J Control Release 153 (2011), 4–15.
54. Riess, J.G., Oxygen carriers (“blood substitutes”): Raison d'etre, chemistry, and some physiology. Chem Rev 101 (2001), 2797–2919.
55. Sakiyama-Elbert, S.E., Hubbell, J.A., Controlled release of nerve growth factor from a heparin-containing fibrin-based cell ingrowth matrix. J Control Release 69 (2000), 149–158.
56. Sakiyama-Elbert, S.E., Hubbell, J.A., Development of fibrin derivatives for controlled release of heparin-binding growth factors. J Control Release 65 (2000), 389–402.
57. Satyam, A., Kumar, P., Fan, X.L., Gorelov, A., Rochev, Y., Joshi, L., Peinado, H., Lyden, D., Thomas, B., Rodriguez, B., Raghunath, M., Pandit, A., Zeugolis, D., Macromolecular crowding meets tissue engineering by self-assembly: A paradigm shift in regenerative medicine. Adv Mater 26 (2014), 3024–3034.
58. Schad, K.C., Hynynen, K., In vitro characterization of perfluorocarbon droplets for focused ultrasound therapy. Phys Med Biol 55 (2010), 4933–4947.
59. Seliktar, D., Designing cell-compatible hydrogels for biomedical applications. Science 336 (2012), 1124–1128.
60. Shaikh, F.M., Callanan, A., Kavanagh, E.G., Burke, P.E., Grace, P.A., McGloughlin, T.M., Fibrin: A natural biodegradable scaffold in vascular tissue engineering. Cells Tissues Organs 188 (2008), 333–346.
61. Sheeran, P.S., Wong, V.P., Luois, S., McFarland, R.J., Ross, W.D., Feingold, S., Matsunaga, T.O., Dayton, P.A., Decafluorobutane as a phase-change contrast agent for low-energy extravascular ultrasonic imaging. Ultrasound Med Biol 37 (2011), 1518–1530.
62. Shpak, O., Stricker, L., Kokhuis, T., Luan, Y., Fowlkes, B., Fabiilli, M., Lohse, D., de Jong, N., Versluis, M., Ultrafast dynamics of the acoustic vaporization of phase-change microdroplets. J Acoust Soc Am, 133, 2013, 3586.
63. Sojo, K., Sawaki, Y., Hattori, H., Mizutani, H., Ueda, M., Immunohistochemical study of vascular endothelial growth factor (VEGF) and bone morphogenetic protein-2, -4 (BMP-2,-4) on lengthened rat femurs. J Cranio-Maxillofac Surg 33 (2005), 238–245.
64. Thornton, P.D., McConnell, G., Ulijn, R.V., Enzyme responsive polymer hydrogel beads. Chem Commun, 2005, 5913–5915.
65. Tse, H.T.K., Weaver, W.M., Di Carlo, D., Increased asymmetric and multi-daughter cell division in mechanically confined microenvironments. PLoS One, 7, 2012, e38986.
66. Unger, E.C., Porter, T., Culp, W., LaBell, R., Matsunaga, T., Zutshi, R., Therapeutic applications of lipid-coated microbubbles. Adv Drug Deliv Rev 56 (2004), 1291–1314.
67. Vangelder, J.M., Nair, C.H., Dhall, D.P., Effects of poloxamer-188 on fibrin network structure, whole-blood clot permeability and fibrinolysis. Thromb Res 71 (1993), 361–376.
68. Ward, M., Wu, J.R., Chiu, J.F., Ultrasound-induced cell lysis and sonoporation enhanced by contrast agents. J Acoust Soc Am 105 (1999), 2951–2957.
69. Whelan, D., Caplice, N.M., Clover, A.J.P., Fibrin as a delivery system in wound healing tissue engineering applications. J Control Release 196 (2014), 1–8.
70. Wong, Z.Z., Kripfgans, O.D., Qamar, A., Fowlkes, J.B., Bull, J.L., Bubble evolution in acoustic droplet vaporization at physiological temperature via ultra-high speed imaging. Soft Matter 7 (2011), 4009–4016.
71. Wu, C., Chen, C., Lai, J., Mu, X., Zheng, J., Zhao, Y., Molecule-scale controlled-release system based on light-responsive silica nanoparticles. Chem Commun 23 (2008), 2662–2664.
72. Zhao, X., Kim, J., Cezar, C.A., Huebsch, N., Lee, K., Bouhadir, K., Mooney, D.J., Active scaffolds for on-demand drug and cell delivery. Proc Natl Acad Sci USA 108 (2011), 67–72.