Multimodal ultrasound-photoacoustic imaging of tissue engineering scaffolds and blood oxygen saturation in and around the scaffolds

Tissue Engineering - Part C: Methods

Volumn 20, Issue 5, 2014, Pages 440-449

  Talukdar, Yahfi ^a   Avti, Pramod ^a   Sun, John ^b   Sitharaman, Balaji ^a  

^a St Francis Hospital The Heart Center   (United States)

^b Sonics Inc   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BIOMATERIALS; BLOOD; COMPUTERIZED TOMOGRAPHY; COPOLYMERS; OXYGEN; PHYSIOLOGICAL MODELS; PHYSIOLOGY; POLYMERS; SINGLE-WALLED CARBON NANOTUBES (SWCN); TISSUE; ULTRASONIC APPLICATIONS; ULTRASONICS;

BLOOD OXYGEN SATURATION; MICROCOMPUTED TOMOGRAPHY; PHYSIOLOGICAL CONDITION; PHYSIOLOGICAL PROCESS; POLY(LACTIC-CO-GLYCOLIC ACID); SCAFFOLD CHARACTERIZATION; SINGLEWALLED CARBON NANOTUBE (SWCNT); TISSUE ENGINEERING SCAFFOLD;

SCAFFOLDS (BIOLOGY);

POLYGLACTIN; SINGLE WALLED NANOTUBE; TISSUE SCAFFOLD; CARBON NANOTUBE; LACTIC ACID; OXYGEN; POLYGLYCOLIC ACID; POLYLACTIC ACID-POLYGLYCOLIC ACID COPOLYMER;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BLOOD OXYGEN TENSION; CHICKEN; EX VIVO STUDY; HISTOLOGY; IMAGING SYSTEM; IN VIVO STUDY; MALE; MULTIMODAL IMAGING; NON INVASIVE PROCEDURE; NONHUMAN; PHOTOACOUSTICS; PRIORITY JOURNAL; RAT; TISSUE ENGINEERING; ULTRASOUND; VASCULARIZATION; ANIMAL; ATOMIC FORCE MICROSCOPY; BLOOD; CHEMISTRY; PROCEDURES; SPRAGUE DAWLEY RAT; TISSUE SCAFFOLD; ULTRASTRUCTURE;

ANIMALS; LACTIC ACID; MALE; MICROSCOPY, ATOMIC FORCE; MULTIMODAL IMAGING; NANOTUBES, CARBON; OXYGEN; PHOTOACOUSTIC TECHNIQUES; POLYGLYCOLIC ACID; RATS, SPRAGUE-DAWLEY; TISSUE ENGINEERING; TISSUE SCAFFOLDS; ULTRASONICS;

EID: 84899555457     PISSN: 19373384     EISSN: 19373392     Source Type: Journal    
DOI: 10.1089/ten.tec.2013.0203     Document Type: Article

References (64)

1. Choi, S.W., Zhang, Y., Thomopoulos, S., and Xia, Y. In vitro mineralization by preosteoblasts in poly(DL-lactide-co-glycolide) inverse opal scaffolds reinforced with hydroxyapatite nanoparticles. Langmuir 26, 12126, 2010.
2. Kim, S.S., Sun Park,M., Jeon, O., Yong Choi, C., and Kim, B.S. Poly (lactide-co-glycolide)/hydroxyapatite composite scaffolds for bone tissue engineering. Biomaterials 27, 1399, 2006.
3. Yoshimoto, H., Shin, Y., Terai, H., and Vacanti, J. A biodegradable nanofiber scaffold by electrospinning and its potential for bone tissue engineering. Biomaterials 24, 2077, 2003.
4. Ge, Z., Baguenard, S., Lim, L.Y., Wee, A., and Khor, E. Hydroxyapatite-chitin materials as potential tissue engineered bone substitutes. Biomaterials 25, 1049, 2004.
5. O'Keefe, R.J., and Mao, J. Bone tissue engineering and regeneration: from discovery to the clinic,A an overview. Tissue Eng Part B Rev 17, 389, 2011.
6. Muzzarelli, R.A., Greco, F., Busilacchi, A., Sollazzo, V., and Gigante, A. Chitosan, hyaluronan and chondroitin sulfate in tissue engineering for cartilage regeneration: a review. Carbohydr Polymers 89, 723, 2012.
7. Atala, A. Tissue engineering of human bladder. Br Med Bull 97, 81, 2011.
8. Burg KJL, Porter, S., and Kellam, J.F. Biomaterial developments for bone tissue engineering. Biomaterials 21, 2347, 2000.
9. Rezwan, K., Chen, Q., Blaker, J., and Boccaccini, A.R. Biodegradable and bioactive porous polymer/inorganic composite scaffolds for bone tissue engineering. Biomaterials 27, 3413, 2006.
10. Zhang, P., Wu, H., Lu, Z., Deng, C., Hong, Z., Jing, X., et al. RGD-conjugated copolymer incorporated into composite of poly(lactide-co- glycotide) and poly(L-lactide)-grafted nanohydroxyapatite for bone tissue engineering. Biomacromolecules, 12, 2667, 2011.
11. Sitharaman, B., Avti, P.K., Schaefer, K., Talukdar, Y., and Longtin, J.P. A novel nanoparticle-enhanced photoacoustic stimulus for bone tissue engineering. Tissue Eng Part A 17, 1851, 2011.
12. Cai, X., Paratala, B.S., Hu, S., Sitharaman, B., and Wang, L.V. Multiscale photoacoustic microscopy of single-walled carbon nanotube- incorporated tissue engineering scaffolds. Tissue Eng Part C Methods 18, 310, 2012.
13. Eltoum, I., Fredenburgh, J., Myers, R.B., and Grizzle, W.E. Introduction to the theory and practice of fixation of tissues. J Histotechnol 24, 173, 2001.
14. Bancroft, J.D., and Gamble, M. Theory and Practice of Histological Techniques. Elsevier Health Sciences; London, UK: Churchill Livingstone, 2008.
15. Dapson, R. Macromolecular changes caused by formalin fixation and antigen retrieval. Biotech Histochem 82, 133, 2007.
16. Risau, W., and Flamme, I. Vasculogenesis. Ann Rev Cell Dev Biol 11, 73, 1995.
17. Druecke, D., Langer, S., Lamme, E., Pieper, J., Ugarkovic, M., Steinau, H.U., et al. Neovascularization of poly(ether ester) block-copolymer scaffolds in vivo: long-term investigations using intravital fluorescent microscopy. J Biomed Mater Res Part A 68, 10, 2004.
18. Kellner, K., Liebsch, G., Klimant, I., Wolfbeis, O.S., Blunk, T., Schulz, M.B., et al. Determination of oxygen gradients in engineered tissue using a fluorescent sensor. Biotechnol Bioeng, 80, 73, 2002.
19. Barrilleaux, B., Phinney, D.G., Prockop, D.J., and O'connor, K.C. Review: ex vivo engineering of living tissues with adult stem cells. Tissue Eng 12, 3007, 2006.
20. D'Ippolito, G., Diabira, S., Howard, G.A., Roos, B.A., and Schiller, P.C. Low oxygen tension inhibits osteogenic differentiation and enhances stemness of human MIAMI cells. Bone 39, 513, 2006.
21. Carrancio, S., and López-Holgado. N, Sánchez-Guijo. FM, Villaró n. E, Barbado. V, Tabera. S, et al. Optimization of mesenchymal stem cell expansion procedures by cell separation and culture conditions modification. Exp Hematol 36, 1014, 2008.
22. Schenke-Layland, K., Riemann, I., Damour, O., Stock, U.A., and Konig, K. Two-photon microscopes and in vivo multiphoton tomographs - Powerful dicagnostic tools for tissue engineering and drug delivery. Adv Drug Deliv Rev 58, 878, 2006.
23. C. C-R, El Haj, A.J., Yang, X., and Yang, Y. Fluorescent labeling of chitosan for use in non-invasive monitoring of degradation in tissue engineering. J Tissue Eng Regenerative Med 7, 39, 2011.
24. Georgakoudi, I., Rice, W.L., Hronik-Tupaj, M., and Kaplan, D.L. Optical spectroscopy and imaging for the noninvasive evaluation of engineered tissues. Tissue Eng Part B Rev 14, 321, 2008.
25. Studwell, A.J., and Kotton, D.N. A Shift From Cell Cultures to Creatures: In vivo imaging of small animals in experimental regenerative medicine. Mol Ther 19, 1933, 2011.
26. Wittenborn, T., Nielsen, T., Nygaard, J.V., Larsen EKU, Thim, T., Rydtoft, L.M., et al. Ultrahigh-field DCE-MRI of angiogenesis in a novel angiogenesis mouse model. J Magn Reson Imaging 35, 703, 2012.
27. Young, S., Kretlow, J.D., Nguyen, C., Bashoura, A.G., Baggett, L.S., Jansen, J.A., et al. Microcomputed tomography characterization of neovascularization in bone tissue engineering applications. Tissue Eng Part B Rev 14, 295, 2008.
28. Rao, B., Maslov, K., Danielli, A., Chen, R., Shung, K.K., Zhou, Q., et al. Real-time four-dimensional optical-resolution photoacoustic microscopy with Au nanoparticle-assisted subdiffraction-limit resolution. Opt Lett 36, 1137, 2011.
29. Chen, W.T., Ting Fang Shih, T., Chen, R.C., Tu, S.Y., Wen- Yuen, H., and Yang, P.C. Integrin alphavbeta3-targeted dynamic contrast-enhanced magnetic resonance imaging using a gadolinium-loaded polyethylene gycol-dendrimercyclic rgd conjugate to evaluate tumor angiogenesis and to assess early antiangiogenic treatment response in a mouse xenograft tumor model. Mol Imaging 11, 286, 2012.
30. Haney, C.R., Fan, X., Markiewicz, E., Mustafi, D., Karczmar, G.S., and Stadler, W.M. A shift from cell cultures to creatures: monitoring anti-angiogenic therapy in colorectal cancer murine model using dynamic contrast-enhanced MRIcomparing pixel-by-pixel with region of interest analysis. Technol Cancer Res Treat 12, 7, 2012.
31. Huang, S.Y., Chen, B.B., Lu, H.Y., Lin, H.H., Wei, S.Y., Hsu, S.C., et al. Correlation among DCE-MRI measurements of bone marrow angiogenesis, microvessel density, and extramedullary disease in patients with multiple myeloma. Am J Hematol 87, 837, 2012.
32. O'Connor JPB, Jackson, A., Parker GJM, and Jayson, G.C. DCE-MRI biomarkers in the clinical evaluation of antiangiogenic and vascular disrupting agents. Br J Cancer 96, 189, 2007.
33. Van Der Zande, M., Sitharaman, B., Walboomers, X.F., Tran, L., Ananta, J.S., Veltien, A., et al. In vivo magnetic resonance imaging of the distribution pattern of gadonanotubes released from a degrading poly (lactic-co-glycolic acid) scaffold. Tissue Eng Part C Methods 17, 19, 2010.
34. Sitharaman, B., Van Der Zande, M., Ananta, J.S., Shi, X., Veltien, A., Walboomers, X.F., et al. Magnetic resonance imaging studies on gadonanotube, reinforced biodegradable polymer nanocomposites. J Biomed Mater Res Part A 93, 1454, 2010.
35. Viator, J.A., Komadina, J., Svaasand, L.O., Aguilar, G., Choi, B., and Nelson, J.S. A comparative study of photoacoustic and reflectance methods for determination of epidermal melanin content. J Invest Dermatol 122, 1432, 2004.
36. Zhang, H.F., Maslov, K., Sivaramakrishnan, M., Stoica, G., and Wang, L.V. Imaging of hemoglobin oxygen saturation variations in single vessels in vivo using photoacoustic microscopy. Appl Phys Lett 90, 053901, 2007.
37. Cai, X., Hu, S., Paratala, B., Sitharaman, B., and Wang, L.V. Dual-mode photoacoustic microscopy of carbon nanotube incorporated scaffolds in blood and biological tissues. Photons Plus Ultrasound Imaging Sensing 7899, 2I, 2011.
38. Pramanik, M., Song, K.H., Swierczewska, M., Green, D., Sitharaman, B., and Wang, L.V. In vivo carbon nanotubeenhanced non-invasive photoacoustic mapping of the sentinel lymph node. Phys Med Biol 54, 3291, 2009.
39. Xiang, L., Yuan, Y., Xing, D., Ou, Z., Yang, S., and Zhou, F. Photoacoustic molecular imaging with antibody-functionalized single-walled carbon nanotubes for early diagnosis of tumor. J Biomed Opt 14, 021007, 2009.
40. Emelianov, S.Y., Li, P.C., and O'Donnell, M. Photoacoustics for molecular imaging and therapy. Phys Today 62, 34, 2009.
41. Hu, S., Maslov, K., and Wang, L.V. Three-dimensional optical- resolution photoacoustic microscopy. J Vis Exp 3, 55, 2011.
42. Aguirre, A., Guo, P., Gamelin, J., Yan, S., Sanders, M.M., Brewer, M., et al. Coregistered three-dimensional ultrasound and photoacoustic imaging system for ovarian tissue characterization. J Biomed Opt 14, 054014, 2009.
43. Bayer, C.L., Joshi, P.P., and Emelianov, S.Y. Photoacoustic imaging: a potential tool to detect early indicators of metastasis. Expert Rev Med Devices 10, 125, 2013.
44. Emelianov, S., Wang, B., Su, J., Karpiouk, A., Yantsen, E., Sokolov, K., et al. Intravascular ultrasound and photoacoustic imaging. Conf Proc IEEE Eng Med Biol Soc 2008, 2, 2008.
45. Mehrmohammadi, M., Yoon, S.J., Yeager, D., and Emelianov, S.Y. Photoacoustic Imaging for Cancer Detection and Staging. Curr Mol Imaging 2, 89-105, 2013.
46. Nam, S.Y., Ricles, L.M., Suggs, L.J., and Emelianov, S.Y. In vivo ultrasound and photoacoustic monitoring of mesenchymal stem cells labeled with gold nanotracers. PLoS One 7, e37267, 2012.
47. Sethuraman, S., Aglyamov, S.R., Amirian, J.H., Smalling, R.W., and Emelianov, S.Y. Intravascular photoacoustic imaging using an IVUS imaging catheter. IEEE Trans Ultrason Ferroelectr Freq Control 54, 978, 2007.
48. Shi, X., Sitharaman, B., Pham, Q.P., Liang, F., Wu, K., Edward Billups, W., et al. Fabrication of porous ultra-short single-walled carbon nanotube nanocomposite scaffolds for bone tissue engineering. Biomaterials 28, 4078, 2007.
49. Lalwani, G., Henslee, A.M., Farshid, B., Lin, L., Kasper, F.K., Qin Y-X, et al. Two-dimensional nanostructure-reinforced biodegradable polymeric nanocomposites for bone tissue engineering. Biomacromolecules 14, 900, 2013.
50. Lalwani, G., Kwaczala, A.T., Kanakia, S., Patel, S.C., Judex, S., and Sitharaman, B. Fabrication and characterization of three-dimensional macroscopic all-carbon scaffolds. Carbon N Y 53, 90, 2013.
51. Li, C., Wang, L.V. Photoacoustic tomography and sensing in biomedicine. Phys Med Biol 54, R59, 2009.
52. Shi, X.F., Sitharaman, B., Pham, Q.P., Spicer, P.P., Hudson, J.L., Wilson, L.J., et al. In vitro cytotoxicity of single-walled carbon nanotube/biodegradable polymer nanocomposites. J Biomed Mater Res Part A 86A, 813, 2008.
53. Sitharaman, B., Shi, X.F., Walboomers, X.F., Liao, H.B., Cuijpers, V.,Wilson, L.J., et al. In vivo biocompatibility of ultra-short single-walled carbon nanotube/biodegradable polymer nanocomposites for, bone tissue engineering. Bone 43, 362, 2008.
54. Shi, X., Hudson, J.L., Spicer, P.P., Tour, J.M., Krishnamoorti, R., and Mikos, A.G. Injectable nanocomposites of singlewalled carbon nanotubes and biodegradable polymers for bone tissue engineering. Biomacromolecules 7, 2237, 2006.
55. Sitharaman, B., Shi, X., Tran, L.A., Spicer, P.P., Rusakova, I., Wilson, L.J., et al. Injectable in situ cross-linkable nanocomposites of biodegradable polymers and carbon nanostructures for bone tissue engineering. J Biomater Sci Polymer Edition 18, 655, 2007.
56. Avti, P.K., Hu, S., Favazza, C., Mikos, A.G., Jansen, J.A., Shroyer, K.R., et al. Detection, mapping, and quantification of single walled carbon nanotubes in histological specimens with photoacoustic microscopy. PloS One 7, e35064, 2012.
57. König, K. Multiphoton microscopy in life sciences. J Microsc 200, 83, 2000.
58. De La Zerda, A., Zavaleta, C., Keren, S., Vaithilingam, S., Bodapati, S., Liu, Z., et al. Carbon nanotubes as photoacoustic molecular imaging agents in living mice. Nat Nanotechnol 3, 557, 2008.
59. Cai, X., Zhang, Y., Li, L., Choi, S.W., MacEwan, M.R., Yao, J., et al. Investigation of neovascularization in three-dimensional porous scaffolds in vivo by a combination of multiscale photoacoustic microscopy and optical coherence tomography. Tissue Eng Part C Methods 19, 196, 2012.
60. Maslov, K., Zhang, H.F., Hu, S., and Wang, L.V. Opticalresolution photoacoustic microscopy for in vivo imaging of single capillaries. Opt Lett 33, 929, 2008.
61. Chen, Q., Chen, H., Zheng, D., Kuang, C., Fang, H., Zou, B., et al. Smad7 is required for the development and function of the heart. J Biol Chem 284, 292, 2009.
62. Chance, B., Borer, E., Evans, A., Holtom, G., Kent, J., Maris, M., et al. Optical and Nuclear Magnetic Resonance Studies of Hypoxia in Human Tissue and Tumors. Ann N Y Acad Sci 551, 1, 1988.
63. Kim, S., Chen, Y.S., Luke, G.P., and Emelianov, S.Y. In vivo three-dimensional spectroscopic photoacoustic imaging for monitoring nanoparticle delivery. Biomed Opt Expr 2, 2540, 2011.
64. Koo, V., Hamilton, P., and Williamson, K. Non-invasive in vivo imaging in small animal research. Anal Cell Pathol 28, 127, 2006.