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Biotechnology Letters

, Volume 36, Issue 3, pp 403–415 | Cite as

Imaging the hard/soft tissue interface

  • Alistair Bannerman
  • Jennifer Z. Paxton
  • Liam M. GroverEmail author
Review

Abstract

Interfaces between different tissues play an essential role in the biomechanics of native tissues and their recapitulation is now recognized as critical to function. As a consequence, imaging the hard/soft tissue interface has become increasingly important in the area of tissue engineering. Particularly as several biotechnology based products have made it onto the market or are close to human trials and an understanding of their function and development is essential. A range of imaging modalities have been developed that allow a wealth of information on the morphological and physical properties of samples to be obtained non-destructively in vivo or via destructive means. This review summarizes the use of a selection of imaging modalities on interfaces to date considering the strengths and weaknesses of each. We will also consider techniques which have not yet been utilized to their full potential or are likely to play a role in future work in the area.

Keywords

Biomechanics Enthesis Interface Imaging Native tissues Osteochondral junction Osteotendinous junction 

Notes

Acknowledgments

The authors would like to the acknowledge the following for support and funding: Engineering and Physical Sciences Research Council, and Biotechnology and Biological Sciences Research Council Project number BB/G022356/1 and Orthopedic Research UK, Project number 472.

References

  1. Adams Jr SB, Roberts MJ, Patel NA, Plummer S, Rogowska J, Stamper DL, Fujimoto JG, Brezinski ME, (2003) The use of polarization sensitive optical coherence tomography and elastography to assess connective tissue. Lasers and Electro-Optics, 2003. Conf. on Lasers and Electro-Optics, CLEO ‘03. 1–6 June 2003Google Scholar
  2. Aydin SZ, Bas E, Basci O, Filippucci E, Wakefield RJ, Celikel C, Karahan M, Atagunduz P, Benjamin M, Direskeneli H (2010) Validation of ultrasound imaging for Achilles entheseal fibrocartilage in bovines and description of changes in humans with spondyloarthritis. Ann Rheum Dis 69:2165–2168PubMedCrossRefGoogle Scholar
  3. Bae WC, Dwek JR, Znamirowski R, Statum SM, Hermida JC, D’Lima DD, Sah RL, Du J, Chung CB (2010) Ultrashort echo time MR imaging of osteochondral junction of the knee at 3 T: identification of anatomic structures contributing to signal intensity. Radiology 254:837–845PubMedCentralPubMedCrossRefGoogle Scholar
  4. Barton JK, Guzman F, Tumlinson A (2004) Dual modality instrument for simultaneous optical coherence tomography imaging and fluorescence spectroscopy. J Biomed Opt 9:618–623PubMedCrossRefGoogle Scholar
  5. Benjamin M, Bydder GM (2007) Magnetic resonance imaging of entheses using ultrashort TE (UTE) pulse sequences. J Magn Reson Imaging 25:381–389PubMedCrossRefGoogle Scholar
  6. Benjamin M, McGonagle D (2009) Entheses: tendon and ligament attachment sites. Scand J Med Sci Sports 19:520–527PubMedCrossRefGoogle Scholar
  7. Benjamin M, Moriggl B, Brenner E, Emery P, McGonagle D, Redman S (2004) The “enthesis organ” concept: why enthesopathies may not present as focal insertional disorders. Arthritis Rheum 50:3306–3313PubMedCrossRefGoogle Scholar
  8. Benjamin M, Toumi H, Ralphs JR, Bydder G, Best TM, Milz S (2006) Where tendons and ligaments meet bone: attachment sites ‘entheses’ in relation to exercise and/or mechanical load. J Anat 208:471–490PubMedCentralPubMedCrossRefGoogle Scholar
  9. Benjamin M, Milz S, Bydder GM (2008a) Magnetic resonance imaging of entheses. Part 1. Clin Radiol 63:691–703PubMedCrossRefGoogle Scholar
  10. Benjamin M, Milz S, Bydder GM (2008b) Magnetic resonance imaging of entheses. Part 2. Clin Radiol 63:704–711PubMedCrossRefGoogle Scholar
  11. Brezinski ME, Liu B (2008) Nonlocal quantum macroscopic superposition in a high-thermal low-purity state. Phys Rev A 78:063824CrossRefGoogle Scholar
  12. Bydder M, Rahal A, Fullerton GD, Bydder GM (2007) The magic angle effect: a source of artifact, determinant of image contrast, and technique for imaging. J Magn Reson Imaging 25:290–300PubMedCrossRefGoogle Scholar
  13. Campbell SE, Ferguson VL, Hurley DC (2012) Nanomechanical mapping of the osteochondral interface with contact resonance force microscopy and nanoindentation. Acta Biomater 8:4389–4396PubMedCrossRefGoogle Scholar
  14. Caspers PJ, Lucassen GW, Puppels GJ (2003) Combined in vivo confocal Raman spectroscopy and confocal microscopy of human skin. Biophys J 85:572–580PubMedCentralPubMedCrossRefGoogle Scholar
  15. Chamberland DL, Agarwal A, Kotov N, Fowlkes JR, Carson PL, Wang X (2008) Photoacoustic tomography of joints aided by an Etanercept-conjugated gold nanoparticle contrast agent—an ex vivo preliminary rat study. Nanotechnology 19:095101PubMedCrossRefGoogle Scholar
  16. Chesnick IE, Fowler CB, Mason JT, Potter K (2011) Novel mineral contrast agent for magnetic resonance studies of bone implants grown on a chick chorioallantoic membrane. Magn Reson Imaging 29:1244–1254PubMedCrossRefGoogle Scholar
  17. Clark J, Stechschulte DJ (1998) The interface between bone and tendon at an insertion site: a study of the quadriceps tendon insertion. J Anat 192:605–616PubMedCentralPubMedCrossRefGoogle Scholar
  18. Coates LC, Hodgson R, Conaghan PG, Freeston JE (2012) MRI and ultrasonography for diagnosis and monitoring of psoriatic arthritis. Best Pract Res Clin Rheumatol 26:805–822PubMedCrossRefGoogle Scholar
  19. Day JPR, Domke KF, Rago G, Kano H, Hamaguchi H, Vartiainen EM, Bonn M (2011) Quantitative coherent anti-stokes raman scattering (CARS) microscopy. J Phys Chem B 115:7713–7725PubMedCrossRefGoogle Scholar
  20. Deehan DJ, Cawston TE (2005) The biology of integration of the anterior cruciate ligament. J Bone Joint Surg 87:889–895CrossRefGoogle Scholar
  21. Deng K, Sun C, Liu C, Ma R (2009) Initial experience with visualizing hand and foot tendons by dual-energy computed tomography. Clin Imaging 33:384–389PubMedCrossRefGoogle Scholar
  22. Dieing T, Hollricher O, Toporski J (2011) Confocal Raman microscopy. Springer, New YorkCrossRefGoogle Scholar
  23. Driehuys B, Nouls J, Badea A, Bucholz E, Ghaghada K, Petiet A, Hedlund LW (2008) Small animal imaging with magnetic resonance microscopy. ILAR J 49:35–53PubMedCentralPubMedCrossRefGoogle Scholar
  24. Du J, Pak BC, Znamirowski R, Statum S, Takahashi A, Chung CB, Bydder GM (2005) Magic angle effect in magnetic resonance imaging of the Achilles tendon and enthesis. Magn Reson Imaging 27:557–564CrossRefGoogle Scholar
  25. Ducher G, Cook J, Spurrier D, Coombs P, Ptasznik R, Black J, Bass S (2010) Ultrasound imaging of the patellar tendon attachment to the tibia during puberty: a 12-month follow-up in tennis players. Scan J Med Sci Sports 20:35–40CrossRefGoogle Scholar
  26. Eder L, Barzilai M, Peled N, Gladman DD, Zisman D (2012) The use of ultrasound for the assessment of enthesitis in patients with spondyloarthritis. Clin Radiol 68:219–223PubMedCrossRefGoogle Scholar
  27. Fierz FC, Beckmann F, Huser M, Irsen SH, Leukers B, Witte F, Degistirici Ö, Andronache A, Thie M, Müller B (2008) The morphology of anisotropic 3D-printed hydroxyapatite scaffolds. Biomaterials 29:3799–3806PubMedCrossRefGoogle Scholar
  28. Foster FS, Pavlin CJ, Harasiewicz KA, Christopher DA, Turnbull DH (2000) Advances in ultrasound biomicroscopy. Ultrasound Med Biol 26:1–27PubMedCrossRefGoogle Scholar
  29. Gandjbakhch F, Terslev L, Joshua F, Wakefield RJ, Naredo E, D’Agostino MA, Force OUT (2011) Ultrasound in the evaluation of enthesitis: status and perspectives. Arthritis Res Ther 13:R188PubMedCentralPubMedCrossRefGoogle Scholar
  30. Gao J, Messner K (1996) Quantitative comparison of soft tissue-bone interface at chondral ligament insertions in the rabbit knee joint. J Anat 188:367–373PubMedCentralPubMedGoogle Scholar
  31. Gatehouse PD, Bydder GM (2003) Magnetic resonance imaging of short T2 components in tissue. Clin Radiol 58:1–19PubMedCrossRefGoogle Scholar
  32. Gauthier O, Müller R, von Stechow D, Lamy B, Weiss P, Bouler JM, Aguado E, Daculsi G (2005) In vivo bone regeneration with injectable calcium phosphate biomaterial: a three-dimensional micro-computed tomographic, biomechanical and SEM study. Biomaterials 26:5444–5453PubMedCrossRefGoogle Scholar
  33. Genin GM, Kent A, Birman V, Wopenka B, Pasteris JD, Marquez PJ, Thomopoulos S (2009) Functional grading of mineral and collagen in the attachment of tendon to bone. Biophys J 97:976–985PubMedCentralPubMedCrossRefGoogle Scholar
  34. Gudur M, Rao RR, Hsiao YS, Peterson AW, Deng CX, Stegemann JP (2012) Noninvasive, quantitative, spatiotemporal characterization of mineralization in three-dimensional collagen hydrogels using high-resolution spectral ultrasound imaging. Tissue Eng Part C 18:935–946CrossRefGoogle Scholar
  35. Hashimoto Y, Yoshida G, Toyoda H, Takaoka K (2007) Generation of tendon-to-bone interface “enthesis” with use of recombinant BMP-2 in a rabbit model. J Orthop Res 25:1415–1424PubMedCrossRefGoogle Scholar
  36. Hems T, Tillmann B (2000) Tendon entheses of the human masticatory muscles. Anat Embryol 202:201–208PubMedCrossRefGoogle Scholar
  37. Herber RP, Fong J, Lucas SA, Ho SP (2012) Imaging an adapted dentoalveolar complex. Anat Res Int 2012:782571PubMedCentralPubMedGoogle Scholar
  38. Ho SP, Kurylo MP, Fong TK, Lee SSJ, Wagner HD, Ryder MI, Marshall GW (2010) The biomechanical characteristics of the bone-periodontal ligament-cementum complex. Biomaterials 31:6635–6646PubMedCentralPubMedCrossRefGoogle Scholar
  39. Im GI, Ahn JH, Kim SY, Choi BS, Lee SWA (2010) Hyaluronate-atelocollagenB-tricalcium phosphate–hydroxyapatite biphasic scaffold for the repair of osteochondral defects: a porcine study. Tissue Eng Part A 16:1189–1200PubMedCrossRefGoogle Scholar
  40. Ismail EC, Kaabar W, Garrity D, Gundogdu O, Bunk O, Pfeiffer F, Farquharson MJ, Bradley DA (2010) X-ray phase contrast imaging of the bone-cartilage interface. Appl Radiat Isot 68:767–771PubMedCrossRefGoogle Scholar
  41. Jeffery NS, Stephenson RS, Gallagher JA, Jarvis JC, Cox PG (2011) Micro-computed tomography with iodine staining resolves the arrangement of muscle fibres. J Biomech 44:189–192PubMedCrossRefGoogle Scholar
  42. Johnson TRC, Krauss B, Sedlmair M, Grasruck M, Bruder H, Morhard D, Fink C, Weckbach S, Lenhard M, Schmidt B (2007) Material differentiation by dual energy ct: initial experience. Euro Radiol 17:1510–1517CrossRefGoogle Scholar
  43. Jones AC, Arns CH, Sheppard AP, Hutmacher DW, Milthorpe BK, Knackstedt MA (2007) Assessment of bone ingrowth into porous biomaterials using micro-ct. Biomaterials 28:2491–2504PubMedCrossRefGoogle Scholar
  44. Khanarian NT, Jiang J, Wan LQ, Mow VC, Lu HH (2011) A hydrogel-mineral composite scaffold for osteochondral interface tissue engineering. Tissue Eng Part A 18:533–545PubMedCentralPubMedCrossRefGoogle Scholar
  45. Krafft C, Dietzek B, Popp J (2009) Raman and CARS microspectroscopy of cells and tissues. Analyst 134:1046–1057PubMedCrossRefGoogle Scholar
  46. Kreitz S, Dohmen G, Hasken S, Schmitz-Rode T, Mela P, Jockenhoevel S (2011) Nondestructive method to evaluate the collagen content of fibrin-based tissue engineered structures via ultrasound. Tissue Eng Part C 17:1021–1026CrossRefGoogle Scholar
  47. Larkin P (2011) Infrared and Raman spectroscopy; principles and spectral interpretation. Elsevier, OxfordGoogle Scholar
  48. Lin JD, Aloni S, Altoe V, Webb SM, Ryder MI, Ho SP (2012) Elastic discontinuity due to ectopic calcification in a human fibrous joint. Acta Biomater 9:4787–4795PubMedCentralPubMedCrossRefGoogle Scholar
  49. Liu B, Vercollone C, Brezinski ME (2012) Towards improved collagen assessment: polarization-sensitive optical coherence tomography with tailored reference arm polarization. J Biomed Imaging 2012:892680Google Scholar
  50. Lizzi FL, Feleppa EJ, Kaisar Alam S, Deng CX (2003) Ultrasonic spectrum analysis for tissue evaluation. Pattern Recognit Lett 24:637–658CrossRefGoogle Scholar
  51. Longo UG, Franceschi F, Ruzzini L, Rabitti C, Morini S, Maffulli N, Forriol F, Denaro V (2007) Light microscopic histology of supraspinatus tendon ruptures. Knee Surg Sports Traumatol Arthrosc 15:1390–1394PubMedCrossRefGoogle Scholar
  52. Maher JR, Takahata M, Awad HA, Berger AJ (2011) Raman spectroscopy detects deterioration in biomechanical properties of bone in a glucocorticoid-treated mouse model of rheumatoid arthritis. J Biomed Opt 16:087012PubMedCentralPubMedCrossRefGoogle Scholar
  53. McGregor JE, Donald AM (2010) The application of ESEM to biological samples. J Phys Conf Ser 241:012021CrossRefGoogle Scholar
  54. Metscher BD (2009a) MicroCT for comparative morphology: simple staining methods allow high-contrast 3D imaging of diverse non-mineralized animal tissues. BMC Physiol 9:11PubMedCentralPubMedCrossRefGoogle Scholar
  55. Metscher BD (2009b) MicroCT for developmental biology: a versatile tool for high-contrast 3D imaging at histological resolutions. Dev Dyn 238:632–640PubMedCrossRefGoogle Scholar
  56. Milz S, Rufai A, Buettner A, Putz R, Ralphs JR, Benjamin M (2002) Three-dimensional reconstructions of the Achilles tendon insertion in man. J Anat 200:145–152PubMedCentralPubMedCrossRefGoogle Scholar
  57. Moffat KL, Sun WHS, Pena PE, Chahine NO, Doty SB, Ateshian GA, Hung CT, Lu HH (2008) Characterization of the structure–function relationship at the ligament-to-bone interface. Proc Natl Acad Sci 105:7947–7952PubMedCentralPubMedCrossRefGoogle Scholar
  58. Moriggl B, Kumai T, Milz S, Benjamin M (2003) The structure and histopathology of the “enthesis organ” at the navicular insertion of the tendon of tibialis posterior. J Rheumatol 30:508–517PubMedGoogle Scholar
  59. Movasaghi Z, Rehman S, Rehman DIU (2007) Raman spectroscopy of biological tissues. Appl Spectro Rev 42:493–541CrossRefGoogle Scholar
  60. Navratil M, Mabbott GA, Arriaga EA (2006) Chemical microscopy applied to biological systems. Anal Chem 78:4005–4020PubMedCrossRefGoogle Scholar
  61. Nourissat G, Diop A, Maurel N, Salvat C, Dumont S, Pigenet A, Gosset M, Houard X, Berenbaum F (2010) Mesenchymal stem cell therapy regenerates the native bone-tendon junction after surgical repair in a degenerative rat model. PLoS ONE 5:e12248PubMedCentralPubMedCrossRefGoogle Scholar
  62. Oguma H, Murakami G, Takahashi-Iwanaga H, Aoki M, Ishii S (2001) Early anchoring collagen fibers at the bone—tendon interface are conducted by woven bone formation: light microscope and scanning electron microscope observation using a canine model. J Orthop Res 19:873–880PubMedCrossRefGoogle Scholar
  63. Patil CA, Bosschaart N, Keller MD, van Leeuwen TG, Mahadevan-Jansen A (2008) Combined Raman spectroscopy and optical coherence tomography device for tissue characterization. Opt Lett 33:1135–1137PubMedCentralPubMedCrossRefGoogle Scholar
  64. Pawley J (2006) Handbook of biological confocal microscopy. Springer, New YorkCrossRefGoogle Scholar
  65. Paxton JZ, Grover LM, Baar K (2010a) Engineering an in vitro model of a functional ligament from bone to bone. Tissue Eng Part A 16:3515–3525PubMedCrossRefGoogle Scholar
  66. Paxton JZ, Donnelly K, Keatch RP, Baar K, Grover LM (2010b) Factors affecting the longevity and strength in an in vitro model of the bone-ligament interface. Ann Biomed Eng 38:2155–2166PubMedCentralPubMedCrossRefGoogle Scholar
  67. Paxton JZ, Baar K, Grover LM (2012) Current progress in enthesis repair: strategies for interfacial tissue engineering. Orthop Muscular Syst S1:003Google Scholar
  68. Penel G, Delfosse C, Descamps M, Leroy G (2005) Composition of bone and apatitic biomaterials as revealed by intravital Raman microspectroscopy. Bone 36:893–901PubMedCrossRefGoogle Scholar
  69. Podoleanu AG (2005) Optical coherence tomography. Br J Radiol 78:976–988PubMedCrossRefGoogle Scholar
  70. Rashidifard C, Martin SD, Kumar N, Azimi E, Liu B, Brezinski ME (2012) Single detector polarization-sensitive optical coherence tomography for assessment of rotator cuff tendon integrity. Am J Orthop 48:351–357Google Scholar
  71. Rashidifard C, Vercollone C, Martin S, Liu B, Brezinski ME (2013) The application of optical coherence tomography in musculoskeletal disease. Arthritis 2013:563268PubMedCentralPubMedCrossRefGoogle Scholar
  72. Rice MA, Waters KR, Anseth KS (2009) Ultrasound monitoring of cartilaginous matrix evolution in degradable PEG hydrogels. Acta Biomater 5:152–161PubMedCentralPubMedCrossRefGoogle Scholar
  73. Ritman EL (2011) Current status of developments and applications of micro-CT. Annu Rev Biomed Eng 13:531–552PubMedCrossRefGoogle Scholar
  74. Robson MD, Benjamin M, Gishen P, Bydder GM (2004) Magnetic resonance imaging of the Achilles tendon using ultrashort TE (UTE) pulse sequences. Clin Radiol 59:727–735PubMedCrossRefGoogle Scholar
  75. Rogowska J, Brezinski ME (2002) Image processing techniques for noise removal, enhancement and segmentation of cartilage OCT images. Phys Med Biol 47:641–655PubMedCrossRefGoogle Scholar
  76. Rosenthal J, Mangal V, Walker D, Bennett M, Mohun TJ, Lo CW (2004) Rapid high resolution three dimensional reconstruction of embryos with episcopic fluorescence image capture. Birth Defects Res Part C 72:213–223CrossRefGoogle Scholar
  77. Rufai A, Ralphs JR, Benjamin M (1996) Ultrastructure of fibrocartilages at the insertion of the rat Achilles tendon. J Anat 189:185–191PubMedCentralPubMedGoogle Scholar
  78. Schwartz AG, Pasteris JD, Genin GM, Daulton TL, Thomopoulos S (2012) Mineral distributions at the developing tendon enthesis. PLoS ONE 11:e48630CrossRefGoogle Scholar
  79. Sharpe J (2004) Optical projection tomography. Amu Rev Biomed Eng 6:209–228CrossRefGoogle Scholar
  80. Shaw HM, Vazquez OT, McGonagle D, Bydder G, Santer RM, Benjamin M (2008) Development of the human Achilles tendon enthesis organ. J Anat 213:718–724PubMedCentralPubMedCrossRefGoogle Scholar
  81. Spalazzi JP, Doty SB, Moffat KL, Levine WN, Lu HH (2006) Development of controlled matrix heterogeneity on a triphasic scaffold for orthopedic interface tissue engineering. Tissue Eng 12:3497–3508PubMedCrossRefGoogle Scholar
  82. Spalazzi JP, Dagher E, Doty SB, Guo XE, Rodeo SA, Lu HH (2008) In vivo evaluation of a multiphased scaffold designed for orthopaedic interface tissue engineering and soft tissue-to-bone integration. J Biomed Mater Res A 86:1–12PubMedCrossRefGoogle Scholar
  83. Spindler KP, Wright RW (2008) Anterior cruciate ligament tear. N Engl J Med 359:2135–2142PubMedCentralPubMedCrossRefGoogle Scholar
  84. Sun C, Miao F, Wang X, Wang T, Ma R, Wang D, Liu C (2008) An initial qualitative study of dual-energy CT in the knee ligaments. Surg Radiol Anat 30:443–447PubMedCrossRefGoogle Scholar
  85. Suzuki D, Murakami G, Minoura N (2002) Histology of the bone-tendon interfaces of limb muscles in lizards. Ann Anat 184:363–377PubMedCrossRefGoogle Scholar
  86. Suzuki D, Murakami G, Minoura N (2003) Crocodilian bone-tendon and bone-ligament interfaces. Ann Anat 185:425–433PubMedCrossRefGoogle Scholar
  87. Ventura M, Sun Y, Rusu V, Laverman P, Borm P, Heerschap A, Oosterwijk E, Boerman OC, Jansen JA, Walboomers XF (2012) Dual contrast agent for computed tomography and magnetic resonance hard tissue imaging. Tissue Eng Part C 19:405–416CrossRefGoogle Scholar
  88. Vidal M, Amigo JM (2012) Pre-processing of hyperspectral images. Essential steps before image analysis. Chemom Intell Lab Syst 117:138–148CrossRefGoogle Scholar
  89. Villegas DF, Donahue TLH (2010) Collagen morphology in human meniscal attachments: a SEM study. Connect Tissue Res 51:327–336PubMedCrossRefGoogle Scholar
  90. Votteler M, Carvajal Berrio DA, Pudlas MvWalles H, Stock UA, Schenke-Layland K (2011) Raman spectroscopy for the non-contact and non-destructive monitoring of collagen damage within tissues. J Biophoton 5:47–56CrossRefGoogle Scholar
  91. Vunjak-Novakovic G, Altman G, Horan R, Kaplan DL (2004) Tissue engineering of ligaments. Annu Rev Biomed Eng 6:131–156PubMedCrossRefGoogle Scholar
  92. Weninger WJ, Geyer SH, Mohun TJ, Rasskin-Gutman D, Matsui T, Ribeiro I, Costa LF, Izpisua-Belmonte JC, Müller GB (2006) High-resolution episcopic microscopy: a rapid technique for high detailed 3D analysis of gene activity in the context of tissue architecture and morphology. Anat Embryol 211:213–221PubMedCrossRefGoogle Scholar
  93. Wiell C, Szkudlarek M, Hasselquist M, Møller JM, Nørregaard J, Terslev L, Østergaard M (2012) Power Doppler ultrasonography of painful Achilles tendons and entheses in patients with and without spondyloarthropathy—a comparison with clinical examination and contrast-enhanced MRI. Clin Rheumatol 32:301–308PubMedCrossRefGoogle Scholar
  94. Wopenka B, Kent A, Pasteris JD, Yoon Y, Thomopoulos S (2008) The tendon-to-bone transition of the rotator cuff: a preliminary Raman spectroscopic study documenting the gradual mineralization across the insertion in rat tissue samples. Appl Spectrosc 62:1285–1294PubMedCentralPubMedCrossRefGoogle Scholar
  95. Yang PJ, Temenoff JS (2009) Engineering orthopedic tissue interfaces. Tissue Eng Part B Rev 15:127–141PubMedCentralPubMedCrossRefGoogle Scholar
  96. Yilgor C, Yilgor Huri P, Huri G (2012) Tissue Engineering Strategies in Ligament Regeneration. Stem Cells Int 2012:374676PubMedCentralPubMedCrossRefGoogle Scholar
  97. Yuan S, Roney CA, Wierwille J, Chen CW, Xu B, Griffiths G, Jiang J, Ma H, Cable A, Summers RM (2009) Co-registered optical coherence tomography and fluorescence molecular imaging for simultaneous morphological and molecular imaging. Phys Med Biol 55:191CrossRefGoogle Scholar
  98. Zheng YP, Bridal SL, Shi J, Saied A, Lu MH, Jaffre B, Mak AFT, Laugier P (2004) High resolution ultrasound elastomicroscopy imaging of soft tissues: system development and feasibility. Phys Med Biol 49:3925–3938PubMedCrossRefGoogle Scholar
  99. Zipfel WR, Williams RM, Christie R, Nikitin AY, Hyman BT, Webb WW (2003) Live tissue intrinsic emission microscopy using multiphoton-excited native fluorescence and second harmonic generation. Proc Natl Acad Sci 100:7075–7080PubMedCentralPubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  • Alistair Bannerman
    • 1
  • Jennifer Z. Paxton
    • 1
  • Liam M. Grover
    • 1
    Email author
  1. 1.School of Chemical EngineeringUniversity of BirminghamBirminghamUK

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