Table of Contents Author Guidelines Submit a Manuscript
Stem Cells International
Volume 2017, Article ID 1836960, 10 pages
https://doi.org/10.1155/2017/1836960
Research Article

Quantitative Assessment of Optimal Bone Marrow Site for the Isolation of Porcine Mesenchymal Stem Cells

1United States Army Institute of Surgical Research, Fort Sam, Houston, TX, USA
2The Geneva Foundation, Tacoma, WA, USA

Correspondence should be addressed to B. Antebi; lim.liam@rtc.ibetna.neb

Received 3 November 2016; Accepted 28 March 2017; Published 30 April 2017

Academic Editor: Marc L. Turner

Copyright © 2017 J. S. McDaniel 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. D. J. Prockop, “Marrow stromal cells as stem cells for nonhematopoietic tissues,” Science, vol. 276, no. 5309, pp. 71–74, 1997. View at Publisher · View at Google Scholar · View at Scopus
  2. Y. Jiang, B. N. Jahagirdar, R. L. Reinhardt et al., “Pluripotency of mesenchymal stem cells derived from adult marrow,” Nature, vol. 418, no. 6893, pp. 41–49, 2002. View at Publisher · View at Google Scholar · View at Scopus
  3. A. I. Caplan and D. Correa, “The MSC: an injury drugstore,” Cell Stem Cell, vol. 9, no. 1, pp. 11–15, 2011. View at Publisher · View at Google Scholar · View at Scopus
  4. M. B. Murphy, K. Moncivais, and A. I. Caplan, “Mesenchymal stem cells: environmentally responsive therapeutics for regenerative medicine,” Experimental & Molecular Medicine, vol. 45, no. 11, article e54, 2013. View at Publisher · View at Google Scholar · View at Scopus
  5. A. Trounson and C. McDonald, “Stem cell therapies in clinical trials: progress and challenges,” Cell Stem Cell, vol. 17, no. 1, pp. 11–22, 2015. View at Publisher · View at Google Scholar · View at Scopus
  6. L. A. McIntyre, D. Moher, D. A. Fergusson et al., “Efficacy of mesenchymal stromal cell therapy for acute lung injury in preclinical animal models: a systematic review,” PloS One, vol. 11, no. 1, article e0147170, 2016. View at Publisher · View at Google Scholar · View at Scopus
  7. A. I. Hoch and J. K. Leach, “Concise review: optimizing expansion of bone marrow mesenchymal stem/stromal cells for clinical applications,” Stem Cells Translational Medicine, vol. 3, no. 5, pp. 643–652, 2014. View at Publisher · View at Google Scholar · View at Scopus
  8. M. F. Pittenger, A. M. Mackay, S. C. Beck et al., “Multilineage potential of adult human mesenchymal stem cells,” Science, vol. 284, no. 5411, pp. 143–147, 1999. View at Publisher · View at Google Scholar · View at Scopus
  9. P. Bianco, S. A. Kuznetsov, M. Riminucci, and R. P. Gehron, “Postnatal skeletal stem cells,” Methods in Enzymology, vol. 419, pp. 117–148, 2006. View at Publisher · View at Google Scholar · View at Scopus
  10. P. Bianco, ““Mesenchymal” stem cells,” Annual Review of Cell and Developmental Biology, vol. 30, pp. 677–704, 2014. View at Publisher · View at Google Scholar · View at Scopus
  11. R. T. van Beem, A. Hirsch, I. M. Lommerse et al., “Recovery and functional activity of mononuclear bone marrow and peripheral blood cells after different cell isolation protocols used in clinical trials for cell therapy after acute myocardial infarction,” EuroIntervention, vol. 4, no. 1, pp. 133–138, 2008. View at Google Scholar
  12. F. H. Seeger, T. Tonn, N. Krzossok, A. M. Zeiher, and S. Dimmeler, “Cell isolation procedures matter: a comparison of different isolation protocols of bone marrow mononuclear cells used for cell therapy in patients with acute myocardial infarction,” European Heart Journal, vol. 28, no. 6, pp. 766–772, 2007. View at Publisher · View at Google Scholar · View at Scopus
  13. M. Aktas, T. F. Radke, B. E. Strauer, P. Wernet, and G. Kogler, “Separation of adult bone marrow mononuclear cells using the automated closed separation system Sepax,” Cytotherapy, vol. 10, no. 2, pp. 203–211, 2008. View at Publisher · View at Google Scholar · View at Scopus
  14. C. Posel, K. Moller, W. Frohlich, I. Schulz, J. Boltze, and D. C. Wagner, “Density gradient centrifugation compromises bone marrow mononuclear cell yield,” PloS One, vol. 7, no. 12, article e50293, 2012. View at Publisher · View at Google Scholar · View at Scopus
  15. N. Jaiswal, S. E. Haynesworth, A. I. Caplan, and S. P. Bruder, “Osteogenic differentiation of purified, culture-expanded human mesenchymal stem cells in vitro,” Journal of Cellular Biochemistry, vol. 64, no. 2, pp. 295–312, 1997. View at Publisher · View at Google Scholar
  16. K. Mareschi, D. Rustichelli, R. Calabrese et al., “Multipotent mesenchymal stromal stem cell expansion by plating whole bone marrow at a low cellular density: a more advantageous method for clinical use,” Stem Cells International, vol. 2012, Article ID 920581, p. 10, 2012. View at Publisher · View at Google Scholar · View at Scopus
  17. P. Horn, S. Bork, A. Diehlmann et al., “Isolation of human mesenchymal stromal cells is more efficient by red blood cell lysis,” Cytotherapy, vol. 10, no. 7, pp. 676–685, 2008. View at Publisher · View at Google Scholar · View at Scopus
  18. P. Horn, S. Bork, and W. Wagner, “Standardized isolation of human mesenchymal stromal cells with red blood cell lysis,” Methods in Molecular Biology, vol. 698, pp. 23–35, 2011. View at Publisher · View at Google Scholar · View at Scopus
  19. L. A. Fortier, H. G. Potter, E. J. Rickey et al., “Concentrated bone marrow aspirate improves full-thickness cartilage repair compared with microfracture in the equine model,” The Journal of Bone and Joint Surgery American Volume, vol. 92, no. 10, pp. 1927–1937, 2010. View at Publisher · View at Google Scholar · View at Scopus
  20. D. Enea, S. Cecconi, S. Calcagno et al., “Single-stage cartilage repair in the knee with microfracture covered with a resorbable polymer-based matrix and autologous bone marrow concentrate,” The Knee, vol. 20, no. 6, pp. 562–569, 2013. View at Publisher · View at Google Scholar · View at Scopus
  21. D. Enea, S. Cecconi, S. Calcagno, A. Busilacchi, S. Manzotti, and A. Gigante, “One-step cartilage repair in the knee: collagen-covered microfracture and autologous bone marrow concentrate. A pilot study,” The Knee, vol. 22, no. 1, pp. 30–35, 2015. View at Publisher · View at Google Scholar · View at Scopus
  22. A. Gigante, S. Cecconi, S. Calcagno, A. Busilacchi, and D. Enea, “Arthroscopic knee cartilage repair with covered microfracture and bone marrow concentrate,” Arthroscopy Techniques, vol. 1, no. 2, pp. e175–e180, 2012. View at Publisher · View at Google Scholar · View at Scopus
  23. A. Gobbi, G. Karnatzikos, C. Scotti, V. Mahajan, L. Mazzucco, and B. Grigolo, “One-step cartilage repair with bone marrow aspirate concentrated cells and collagen matrix in full-thickness knee cartilage lesions: results at 2-year follow-up,” Cartilage, vol. 2, no. 3, pp. 286–299, 2011. View at Publisher · View at Google Scholar · View at Scopus
  24. A. Gobbi, G. Karnatzikos, and S. R. Sankineani, “One-step surgery with multipotent stem cells for the treatment of large full-thickness chondral defects of the knee,” The American Journal of Sports Medicine, vol. 42, no. 3, pp. 648–657, 2014. View at Publisher · View at Google Scholar · View at Scopus
  25. V. Hegde, O. Shonuga, S. Ellis et al., “A prospective comparison of 3 approved systems for autologous bone marrow concentration demonstrated nonequivalency in progenitor cell number and concentration,” Journal of Orthopaedic Trauma, vol. 28, no. 10, pp. 591–598, 2014. View at Publisher · View at Google Scholar · View at Scopus
  26. J. Skowronski and M. Rutka, “Osteochondral lesions of the knee reconstructed with mesenchymal stem cells - results,” Ortopedia, Traumatologia, Rehabilitacja, vol. 15, no. 3, pp. 195–204, 2013. View at Publisher · View at Google Scholar · View at Scopus
  27. R. G. Johnson, “Bone marrow concentrate with allograft equivalent to autograft in lumbar fusions,” Spine (Phila pa 1976), vol. 39, no. 9, pp. 695–700, 2014. View at Publisher · View at Google Scholar · View at Scopus
  28. J. M. Cassano, J. G. Kennedy, K. A. Ross, E. J. Fraser, M. B. Goodale, and L. A. Fortier, “Bone marrow concentrate and platelet-rich plasma differ in cell distribution and interleukin 1 receptor antagonist protein concentration,” Knee Surgery, Sports Traumatology, Arthroscopy, pp. 1–10, 2016. View at Publisher · View at Google Scholar
  29. R. M. Ajiboye, J. T. Hamamoto, M. A. Eckardt, and J. C. Wang, “Clinical and radiographic outcomes of concentrated bone marrow aspirate with allograft and demineralized bone matrix for posterolateral and interbody lumbar fusion in elderly patients,” European Spine Journal, vol. 24, no. 11, pp. 2567–2572, 2015. View at Publisher · View at Google Scholar · View at Scopus
  30. S. Sauerbier, D. Rickert, R. Gutwald et al., “Bone marrow concentrate and bovine bone mineral for sinus floor augmentation: a controlled, randomized, single-blinded clinical and histological trial—per-protocol analysis,” Tissue Engineering. Part a, vol. 17, no. 17-18, pp. 2187–2197, 2011. View at Publisher · View at Google Scholar · View at Scopus
  31. M. Rojas, R. E. Parker, N. Thorn et al., “Infusion of freshly isolated autologous bone marrow derived mononuclear cells prevents endotoxin-induced lung injury in an ex-vivo perfused swine model,” Stem Cell Research & Therapy, vol. 4, no. 2, p. 26, 2013. View at Publisher · View at Google Scholar · View at Scopus
  32. P. Jungbluth, A. R. Hakimi, J. P. Grassmann et al., “The early phase influence of bone marrow concentrate on metaphyseal bone healing,” Injury, vol. 44, no. 10, pp. 1285–1294, 2013. View at Publisher · View at Google Scholar · View at Scopus
  33. L. Zou, X. Zou, L. Chen et al., “Multilineage differentiation of porcine bone marrow stromal cells associated with specific gene expression pattern,” Journal of Orthopaedic Research, vol. 26, no. 1, pp. 56–64, 2008. View at Publisher · View at Google Scholar · View at Scopus
  34. Y. Nakamura, X. Wang, C. Xu et al., “Xenotransplantation of long-term-cultured swine bone marrow-derived mesenchymal stem cells,” Stem Cells, vol. 25, no. 3, pp. 612–620, 2007. View at Publisher · View at Google Scholar · View at Scopus
  35. S. A. Ock, R. Baregundi Subbarao, Y. M. Lee et al., “Comparison of immunomodulation properties of porcine mesenchymal stromal/stem cells derived from the bone marrow, adipose tissue, and dermal skin tissue,” Stem Cells International, vol. 2016, p. 9581350, 2016. View at Publisher · View at Google Scholar · View at Scopus
  36. S. Belenkiy, K. M. Ivey, A. I. Batchinsky et al., “Noninvasive carbon dioxide monitoring in a porcine model of acute lung injury due to smoke inhalation and burns,” Shock (Augusta, Ga), vol. 39, no. 6, pp. 495–500, 2013. View at Google Scholar
  37. B. Antebi, Z. Zhang, Y. Wang, Z. Lu, X. D. Chen, and J. Ling, “Stromal-cell-derived extracellular matrix promotes the proliferation and retains the osteogenic differentiation capacity of mesenchymal stem cells on three-dimensional scaffolds,” Tissue Engineering. Part C, Methods, vol. 21, no. 2, pp. 171–181, 2015. View at Publisher · View at Google Scholar · View at Scopus
  38. C. F. Hyer, G. C. Berlet, B. W. Bussewitz, T. Hankins, H. L. Ziegler, and T. M. Philbin, “Quantitative assessment of the yield of osteoblastic connective tissue progenitors in bone marrow aspirate from the iliac crest, tibia, and calcaneus,” The Journal of Bone and Joint Surgery American Volume, vol. 95, no. 14, pp. 1312–1316, 2013. View at Publisher · View at Google Scholar · View at Scopus
  39. R. F. McLain, J. E. Fleming, C. A. Boehm, and G. F. Muschler, “Aspiration of osteoprogenitor cells for augmenting spinal fusion: comparison of progenitor cell concentrations from the vertebral body and iliac crest,” The Journal of Bone and Joint Surgery American Volume, vol. 87, no. 12, pp. 2655–2661, 2005. View at Publisher · View at Google Scholar · View at Scopus
  40. D. Henrich, C. Nau, S. B. Kraft et al., “Effect of the harvest procedure and tissue site on the osteogenic function of and gene expression in human mesenchymal stem cells,” International Journal of Molecular Medicine, vol. 37, no. 4, pp. 976–988, 2016. View at Publisher · View at Google Scholar · View at Scopus
  41. R. E. Marx and R. Tursun, “A qualitative and quantitative analysis of autologous human multipotent adult stem cells derived from three anatomic areas by marrow aspiration: tibia, anterior ilium, and posterior ilium,” The International Journal of Oral & Maxillofacial Implants, vol. 28, no. 5, pp. e290–e294, 2013. View at Publisher · View at Google Scholar
  42. K. Beitzel, M. B. McCarthy, M. P. Cote et al., “Comparison of mesenchymal stem cells (osteoprogenitors) harvested from proximal humerus and distal femur during arthroscopic surgery,” Arthroscopy, vol. 29, no. 2, pp. 301–308, 2013. View at Publisher · View at Google Scholar · View at Scopus
  43. J. Narbona-Carceles, J. Vaquero, S. Suarez-Sancho, F. Forriol, and M. E. Fernandez-Santos, “Bone marrow mesenchymal stem cell aspirates from alternative sources: is the knee as good as the iliac crest?” Injury, vol. 45, Supplement 4, pp. S42–S47, 2014. View at Publisher · View at Google Scholar · View at Scopus
  44. N. Baker, L. B. Boyette, and R. S. Tuan, “Characterization of bone marrow-derived mesenchymal stem cells in aging,” Bone, vol. 70, pp. 37–47, 2015. View at Publisher · View at Google Scholar · View at Scopus
  45. O. Katsara, L. G. Mahaira, E. G. Iliopoulou et al., “Effects of donor age, gender, and in vitro cellular aging on the phenotypic, functional, and molecular characteristics of mouse bone marrow-derived mesenchymal stem cells,” Stem Cells and Development, vol. 20, no. 9, pp. 1549–1561, 2011. View at Publisher · View at Google Scholar · View at Scopus
  46. G. Siegel, T. Kluba, U. Hermanutz-Klein, K. Bieback, H. Northoff, and R. Schafer, “Phenotype, donor age and gender affect function of human bone marrow-derived mesenchymal stromal cells,” BMC Medicine, vol. 11, p. 146, 2013. View at Publisher · View at Google Scholar · View at Scopus
  47. P. Hernigou, Y. Homma, C. H. Flouzat Lachaniette et al., “Benefits of small volume and small syringe for bone marrow aspirations of mesenchymal stem cells,” International Orthopaedics, vol. 37, no. 11, pp. 2279–2287, 2013. View at Publisher · View at Google Scholar · View at Scopus
  48. G. F. Muschler, C. Boehm, and K. Easley, “Aspiration to obtain osteoblast progenitor cells from human bone marrow: the influence of aspiration volume,” The Journal of Bone and Joint Surgery American Volume, vol. 79, no. 11, pp. 1699–1709, 1997. View at Publisher · View at Google Scholar
  49. M. Gronkjaer, C. F. Hasselgren, A. S. Ostergaard et al., “Bone marrow aspiration: a randomized controlled trial assessing the quality of bone marrow specimens using slow and rapid aspiration techniques and evaluating pain intensity,” Acta Haematologica, vol. 135, no. 2, pp. 81–87, 2016. View at Publisher · View at Google Scholar · View at Scopus
  50. A. Peister, J. A. Mellad, B. L. Larson, B. M. Hall, L. F. Gibson, and D. J. Prockop, “Adult stem cells from bone marrow (MSCs) isolated from different strains of inbred mice vary in surface epitopes, rates of proliferation, and differentiation potential,” Blood, vol. 103, no. 5, pp. 1662–1668, 2004. View at Publisher · View at Google Scholar · View at Scopus
  51. D. G. Phinney, G. Kopen, W. Righter, S. Webster, N. Tremain, and D. J. Prockop, “Donor variation in the growth properties and osteogenic potential of human marrow stromal cells,” Journal of Cellular Biochemistry, vol. 75, no. 3, pp. 424–436, 1999. View at Publisher · View at Google Scholar
  52. F. J. Lv, R. S. Tuan, K. M. Cheung, and V. Y. Leung, “Concise review: the surface markers and identity of human mesenchymal stem cells,” Stem Cells, vol. 32, no. 6, pp. 1408–1419, 2014. View at Publisher · View at Google Scholar · View at Scopus
  53. T. N. Castillo, M. A. Pouliot, H. J. Kim, and J. L. Dragoo, “Comparison of growth factor and platelet concentration from commercial platelet-rich plasma separation systems,” The American Journal of Sports Medicine, vol. 39, no. 2, pp. 266–271, 2011. View at Publisher · View at Google Scholar · View at Scopus
  54. A. Cieslik-Bielecka, D. M. Dohan Ehrenfest, A. Lubkowska, and T. Bielecki, “Microbicidal properties of leukocyte- and platelet-rich plasma/fibrin (L-PRP/L-PRF): new perspectives,” Journal of Biological Regulators and Homeostatic Agents, vol. 26, Supplement 1, no. 2, pp. 43S–52S, 2012. View at Google Scholar
  55. G. Vadala, A. Di Martino, F. Russo et al., “Autologous bone marrow concentrate combined with platelet-rich plasma enhance bone allograft potential to induce spinal fusion,” Journal of Biological Regulators and Homeostatic Agents, vol. 30, no. 4 Suppl 1, pp. 165–172, 2016. View at Google Scholar
  56. R. Hart, M. Komzak, F. Okal, D. Nahlik, P. Jajtner, and M. Puskeiler, “Allograft alone versus allograft with bone marrow concentrate for the healing of the instrumented posterolateral lumbar fusion,” The Spine Journal, vol. 14, no. 7, pp. 1318–1324, 2014. View at Publisher · View at Google Scholar · View at Scopus
  57. E. R. Rodriguez-Collazo and M. L. Urso, “Combined use of the Ilizarov method, concentrated bone marrow aspirate (cBMA), and platelet-rich plasma (PRP) to expedite healing of bimalleolar fractures,” Strategies in Trauma and Limb Reconstruction, vol. 10, no. 3, pp. 161–166, 2015. View at Publisher · View at Google Scholar · View at Scopus
  58. W. Zhong, Y. Sumita, S. Ohba et al., “In vivo comparison of the bone regeneration capability of human bone marrow concentrates vs. platelet-rich plasma,” PloS One, vol. 7, no. 7, article e40833, 2012. View at Publisher · View at Google Scholar · View at Scopus
  59. D. Bharti, S. B. Shivakumar, R. B. Subbarao, and G. J. Rho, “Research advancements in porcine derived mesenchymal stem cells,” Current Stem Cell Research & Therapy, vol. 11, no. 1, pp. 78–93, 2016. View at Publisher · View at Google Scholar
  60. W. A. Noort, M. I. Oerlemans, H. Rozemuller et al., “Human versus porcine mesenchymal stromal cells: phenotype, differentiation potential, immunomodulation and cardiac improvement after transplantation,” Journal of Cellular and Molecular Medicine, vol. 16, no. 8, pp. 1827–1839, 2012. View at Publisher · View at Google Scholar · View at Scopus
  61. M. M. Swindle, A. Makin, A. J. Herron, F. J. Clubb Jr., and K. S. Frazier, “Swine as models in biomedical research and toxicology testing,” Veterinary Pathology, vol. 49, no. 2, pp. 344–356, 2012. View at Publisher · View at Google Scholar · View at Scopus
  62. T. M. Amin and J. A. Sirs, “The blood rheology of man and various animal species,” Quarterly Journal of Experimental Physiology, vol. 70, no. 1, pp. 37–49, 1985. View at Publisher · View at Google Scholar · View at Scopus
  63. I. J. Wallace, G. M. Pagnotti, J. Rubin-Sigler et al., “Focal enhancement of the skeleton to exercise correlates with responsivity of bone marrow mesenchymal stem cells rather than peak external forces,” The Journal of Experimental Biology, vol. 218, Part 19, pp. 3002–3009, 2015. View at Publisher · View at Google Scholar · View at Scopus
  64. S. Sonam, S. R. Sathe, E. K. Yim, M. P. Sheetz, and C. T. Lim, “Cell contractility arising from topography and shear flow determines human mesenchymal stem cell fate,” Scientific Reports, vol. 6, p. 20415, 2016. View at Publisher · View at Google Scholar · View at Scopus
  65. J. Hao, Y. Zhang, D. Jing et al., “Mechanobiology of mesenchymal stem cells: perspective into mechanical induction of MSC fate,” Acta Biomaterialia, vol. 20, pp. 1–9, 2015. View at Publisher · View at Google Scholar · View at Scopus