Table of Contents Author Guidelines Submit a Manuscript
Stem Cells International
Volume 2016, Article ID 1207190, 13 pages
http://dx.doi.org/10.1155/2016/1207190
Research Article

Longitudinal Cell Tracking and Simultaneous Monitoring of Tissue Regeneration after Cell Treatment of Natural Tendon Disease by Low-Field Magnetic Resonance Imaging

1Large Animal Clinic for Surgery, Faculty of Veterinary Medicine, University of Leipzig, An den Tierkliniken 21, 04103 Leipzig, Germany
2Translational Centre for Regenerative Medicine, University of Leipzig, Philipp-Rosenthal-Straße 55, 04103 Leipzig, Germany
3Institute of Veterinary Physiology, University of Leipzig, An den Tierkliniken 7, 04103 Leipzig, Germany

Received 24 July 2015; Revised 24 September 2015; Accepted 20 October 2015

Academic Editor: Phillip C. Yang

Copyright © 2016 Dagmar Berner et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. J. C. Patterson-Kane, D. L. Becker, and T. Rich, “The pathogenesis of tendon microdamage in athletes: the horse as a natural model for basic cellular research,” Journal of Comparative Pathology, vol. 147, no. 2-3, pp. 227–247, 2012. View at Publisher · View at Google Scholar · View at Scopus
  2. D. Kader, A. Saxena, T. Movin, and N. Maffulli, “Achilles tendinopathy: some aspects of basic science and clinical management,” British Journal of Sports Medicine, vol. 36, no. 4, pp. 239–249, 2002. View at Publisher · View at Google Scholar · View at Scopus
  3. B. A. Dowling, A. J. Dart, D. R. Hodgson, and R. K. W. Smith, “Superficial digital flexor tendonitis in the horse,” Equine Veterinary Journal, vol. 32, no. 5, pp. 369–378, 2000. View at Google Scholar · View at Scopus
  4. E. E. Godwin, N. J. Young, J. Dudhia, I. C. Beamish, and R. K. W. Smith, “Implantation of bone marrow-derived mesenchymal stem cells demonstrates improved outcome in horses with overstrain injury of the superficial digital flexor tendon,” Equine Veterinary Journal, vol. 44, no. 1, pp. 25–32, 2012. View at Publisher · View at Google Scholar · View at Scopus
  5. R. K. W. Smith, M. Korda, G. W. Blunn, and A. E. Goodship, “Isolation and implantation of autologous equine mesenchymal stem cells from bone marrow into the superficial digital flexor tendon as a potential novel treatment,” Equine Veterinary Journal, vol. 35, no. 1, pp. 99–102, 2003. View at Google Scholar · View at Scopus
  6. M. Dominici, K. Le Blanc, I. Mueller et al., “Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement,” Cytotherapy, vol. 8, no. 4, pp. 315–317, 2006. View at Publisher · View at Google Scholar · View at Scopus
  7. R. Hass, C. Kasper, S. Böhm, and R. Jacobs, “Different populations and sources of human mesenchymal stem cells (MSC): a comparison of adult and neonatal tissue-derived MSC,” Cell Communication and Signaling, vol. 9, article 12, 2011. View at Publisher · View at Google Scholar · View at Scopus
  8. J. Burk, I. Ribitsch, C. Gittel et al., “Growth and differentiation characteristics of equine mesenchymal stromal cells derived from different sources,” Veterinary Journal, vol. 195, no. 1, pp. 98–106, 2013. View at Publisher · View at Google Scholar · View at Scopus
  9. D. D. Carrade, V. K. Affolter, C. A. Outerbridge et al., “Intradermal injections of equine allogeneic umbilical cord-derived mesenchymal stem cells are well tolerated and do not elicit immediate or delayed hypersensitivity reactions,” Cytotherapy, vol. 13, no. 10, pp. 1180–1192, 2011. View at Publisher · View at Google Scholar · View at Scopus
  10. M. Secco, E. Zucconi, N. M. Vieira et al., “Multipotent stem cells from umbilical cord: cord is richer than blood!,” Stem Cells, vol. 26, no. 1, pp. 146–150, 2008. View at Publisher · View at Google Scholar · View at Scopus
  11. M. A. Vidal, N. J. Walker, E. Napoli, and D. L. Borjesson, “Evaluation of senescence in mesenchymal stem cells isolated from equine bone marrow, adipose tissue, and umbilical cord tissue,” Stem Cells and Development, vol. 21, no. 2, pp. 273–283, 2012. View at Publisher · View at Google Scholar · View at Scopus
  12. A. Crovace, L. Lacitignola, R. de Siena, G. Rossi, and E. Francioso, “Cell therapy for tendon repair in horses: an experimental study,” Veterinary Research Communications, vol. 31, supplement 1, pp. 281–283, 2007. View at Publisher · View at Google Scholar · View at Scopus
  13. L. V. Schnabel, M. E. Lynch, M. C. H. van der Meulen, A. E. Yeager, M. A. Kornatowski, and A. J. Nixon, “Mesenchymal stem cells and insulin-like growth factor-I gene-enhanced mesenchymal stem cells improve structural aspects of healing in equine flexor digitorum superficialis tendons,” Journal of Orthopaedic Research, vol. 27, no. 10, pp. 1392–1398, 2009. View at Publisher · View at Google Scholar · View at Scopus
  14. R. K. W. Smith, “Mesenchymal stem cell therapy for equine tendinopathy,” Disability and Rehabilitation, vol. 30, no. 20–22, pp. 1752–1758, 2008. View at Publisher · View at Google Scholar · View at Scopus
  15. S. Pacini, S. Spinabella, L. Trombi et al., “Suspension of bone marrow-derived undifferentiated mesenchymal stromal cells for repair of superficial digital flexor tendon in race horses,” Tissue Engineering, vol. 13, no. 12, pp. 2949–2955, 2007. View at Publisher · View at Google Scholar · View at Scopus
  16. A. J. Nixon, L. A. Dahlgren, J. L. Haupt, A. E. Yeager, and D. L. Ward, “Effect of adipose-derived nucleated cell fractions on tendon repair in horses with collagenase-induced tendinitis,” American Journal of Veterinary Research, vol. 69, no. 7, pp. 928–937, 2008. View at Publisher · View at Google Scholar · View at Scopus
  17. J. Burk and W. Brehm, “Stem cell therapy of tendon injuries—clinical outcome in 98 cases,” Pferdeheilkunde, vol. 27, no. 2, pp. 153–161, 2011. View at Google Scholar · View at Scopus
  18. D. J. Guest, M. R. W. Smith, and W. R. Allen, “Monitoring the fate of autologous and allogeneic mesenchymal progenitor cells injected into the superficial digital flexor tendon of horses: preliminary study,” Equine Veterinary Journal, vol. 40, no. 2, pp. 178–181, 2008. View at Publisher · View at Google Scholar · View at Scopus
  19. A. Sole, M. Spriet, L. D. Galuppo et al., “Scintigraphic evaluation of intra-arterial and intravenous regional limb perfusion of allogeneic bone marrow-derived mesenchymal stem cells in the normal equine distal limb using Tc99m-HMPAO,” Equine Veterinary Journal, vol. 44, no. 5, pp. 594–599, 2012. View at Publisher · View at Google Scholar · View at Scopus
  20. A. Sole, M. Spriet, K. A. Padgett et al., “Distribution and persistence of technetium-99 hexamethyl propylene amine oxime-labelled bone marrow-derived mesenchymal stem cells in experimentally induced tendon lesions after intratendinous injection and regional perfusion of the equine distal limb,” Equine Veterinary Journal, vol. 45, no. 6, pp. 726–731, 2013. View at Publisher · View at Google Scholar · View at Scopus
  21. M. Spriet, S. Buerchler, J. M. Trela et al., “Scintigraphic tracking of mesenchymal stem cells after intravenous regional limb perfusion and subcutaneous administration in the standing horse,” Veterinary Surgery, vol. 44, no. 3, pp. 273–280, 2015. View at Publisher · View at Google Scholar
  22. B. Addicott, M. Willman, J. Rodriguez et al., “Mesenchymal stem cell labeling and in vitro MR characterization at 1.5 T of new SPIO contrast agent: molday ION Rhodamine-B,” Contrast Media & Molecular Imaging, vol. 6, no. 1, pp. 7–18, 2011. View at Publisher · View at Google Scholar · View at Scopus
  23. U. Delling, W. Brehm, M. Metzger, E. Ludewig, K. Winter, and H. Jülke, “In vivo tracking and fate of intra-articularly injected superparamagnetic iron oxide particle-labeled multipotent stromal cells in an ovine model of osteoarthritis,” Cell Transplantation, vol. 24, no. 11, pp. 2379–2390, 2015. View at Publisher · View at Google Scholar
  24. X.-H. Jing, L. Yang, X.-J. Duan et al., “In vivo MR imaging tracking of magnetic iron oxide nanoparticle labeled, engineered, autologous bone marrow mesenchymal stem cells following intra-articular injection,” Joint Bone Spine, vol. 75, no. 4, pp. 432–438, 2008. View at Publisher · View at Google Scholar · View at Scopus
  25. A. Scharf, S. Holmes, M. Thoresen, J. Mumaw, A. Stumpf, and J. Peroni, “Superparamagnetic iron oxide nanoparticles as a means to track mesenchymal stem cells in a large animal model of tendon injury,” Contrast Media & Molecular Imaging, vol. 10, no. 5, pp. 388–397, 2015. View at Publisher · View at Google Scholar
  26. Y. Yang, J. Zhang, Y. Qian et al., “Superparamagnetic Iron oxide is suitable to label tendon stem cells and track them in vivo with Mr imaging,” Annals of Biomedical Engineering, vol. 41, no. 10, pp. 2109–2119, 2013. View at Publisher · View at Google Scholar · View at Scopus
  27. J. K. Harrington, H. Chahboune, J. M. Criscione et al., “Determining the fate of seeded cells in venous tissue-engineered vascular grafts using serial MRI,” The FASEB Journal, vol. 25, no. 12, pp. 4150–4161, 2011. View at Publisher · View at Google Scholar · View at Scopus
  28. H. Jülke, C. Veit, I. Ribitsch, W. Brehm, E. Ludewig, and U. Delling, “Comparative labeling of equine and ovine multipotent stromal cells with superparamagnetic iron oxide particles for magnetic resonance imaging in vitro,” Cell Transplantation, vol. 24, no. 6, pp. 1111–1125, 2015. View at Google Scholar
  29. Y.-G. Li, J.-N. Wei, J. Lu, X.-T. Wu, and G.-J. Teng, “Labeling and tracing of bone marrow mesenchymal stem cells for tendon-to-bone tunnel healing,” Knee Surgery, Sports Traumatology, Arthroscopy, vol. 19, no. 12, pp. 2153–2158, 2011. View at Publisher · View at Google Scholar · View at Scopus
  30. S. C. Berman, C. Galpoththawela, A. A. Gilad, J. W. M. Bulte, and P. Walczak, “Long-term MR cell tracking of neural stem cells grafted in immunocompetent versus immunodeficient mice reveals distinct differences in contrast between live and dead cells,” Magnetic Resonance in Medicine, vol. 65, no. 2, pp. 564–574, 2011. View at Publisher · View at Google Scholar · View at Scopus
  31. C. A. Bourzac, J. B. Koenig, K. A. Link, S. G. Nykamp, and T. G. Koch, “Evaluation of ultrasmall superparamagnetic iron oxide contrast agent labeling of equine cord blood and bone marrow mesenchymal stromal cells,” American Journal of Veterinary Research, vol. 75, no. 11, pp. 1010–1017, 2014. View at Publisher · View at Google Scholar · View at Scopus
  32. F. Paebst, D. Piehler, W. Brehm et al., “Comparative immunophenotyping of equine multipotent mesenchymal stromal cells: an approach toward a standardized definition,” Cytometry Part A, vol. 85, no. 8, pp. 678–687, 2014. View at Publisher · View at Google Scholar · View at Scopus
  33. J. Burk, C. Gittel, S. Heller et al., “Gene expression of tendon markers in mesenchymal stromal cells derived from different sources,” BMC Research Notes, vol. 7, no. 1, article 826, 2014. View at Publisher · View at Google Scholar
  34. N. W. Rantanen, J. S. Jorgensen, and R. L. Genovese, “Ultrasonographic evaluation of the equine limb: technique,” in Diagnosis and Management of Lameness in the Horse, M. W. Ross and S. J. Dyson, Eds., pp. 182–205, Saunders, 2nd edition, 2010. View at Google Scholar
  35. S. A. Vallance, M. A. Vidal, M. B. Whitcomb, B. G. Murphy, M. Spriet, and L. D. Galuppo, “Evaluation of a diode laser for use in induction of tendinopathy in the superficial digital flexor tendon of horses,” American Journal of Veterinary Research, vol. 73, no. 9, pp. 1435–1444, 2012. View at Publisher · View at Google Scholar · View at Scopus
  36. E. Küstermann, U. Himmelreich, K. Kandal et al., “Efficient stem cell labeling for MRI studies,” Contrast Media & Molecular Imaging, vol. 3, no. 1, pp. 27–37, 2008. View at Publisher · View at Google Scholar · View at Scopus
  37. D. J. Guest, M. R. W. Smith, and W. R. Allen, “Equine embryonic stem-like cells and mesenchymal stromal cells have different survival rates and migration patterns following their injection into damaged superficial digital flexor tendon,” Equine Veterinary Journal, vol. 42, no. 7, pp. 636–642, 2010. View at Publisher · View at Google Scholar · View at Scopus
  38. M. Spriet, K. A. Padgett, M. A. Vidal, L. D. Galuppo, and E. R. Wisner, “Comparison of low-field and high-field MRI for the in vitro detection of iron oxides labeled mesenchymal stem cells,” in Proceedings of the Annual European Veterinary Diagnostic Imaging Meeting (EVDI '13), p. 58, Cascais, Portugal, August-September 2013.
  39. J. Burk, I. Erbe, D. Berner et al., “Freeze-thaw cycles enhance decellularization of large tendons,” Tissue Engineering Part C: Methods, vol. 20, no. 4, pp. 276–284, 2014. View at Publisher · View at Google Scholar · View at Scopus
  40. G. D. Fullerton, I. L. Cameron, and V. A. Ord, “Orientation of tendons in the magnetic field and its effect on T2 relaxation times,” Radiology, vol. 155, no. 2, pp. 433–435, 1985. View at Publisher · View at Google Scholar · View at Scopus
  41. J. Burk, C. Horstmeier, A. Ahrberg, A. Hillmann, K. Winter, and W. Brehm, “Longitudinal cell tracking by magnetic resonance imaging following treatment of induced tendon lesions,” in Proceedings of the 4th TERMIS World Congress, Boston, Mass, USA, September 2015, Tissue Engineering Part A, vol. 21, supplement 1, p. S-49, 2015.
  42. W. M. Karlin, A. A. Stewart, S. S. Durgam, J. F. Naughton, K. J. O'dell-Anderson, and M. C. Stewart, “Evaluation of experimentally induced injury to the superficial digital flexor tendon in horses by use of low-field magnetic resonance imaging and ultrasonography,” American Journal of Veterinary Research, vol. 72, no. 6, pp. 791–798, 2011. View at Publisher · View at Google Scholar · View at Scopus
  43. M. Schramme, S. Hunter, N. Campbell, A. Blikslager, and R. K. W. Smith, “A surgical tendonitis model in horses: technique, clinical, ultrasonographic and histological characterisation,” Veterinary and Comparative Orthopaedics and Traumatology, vol. 23, no. 4, pp. 231–239, 2010. View at Publisher · View at Google Scholar · View at Scopus