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Osteogenic Potential of the Periosteum and Periosteal Augmentation for Bone-tunnel Healing  

Youn Inchan (Department of Surgery Orthopaedic Research Laboratory Duke University)
Suh J-K Francis (Department of Biomedical Engineering Tulane University)
Choi Kuiwon (Korea Institute Science and Technology Biomedical Research Center)
Publication Information
Journal of Biomedical Engineering Research / v.26, no.2, 2005 , pp. 101-110 More about this Journal
Abstract
Periosteum and periosteum-derived progenitor cells have demonstrated the potential for stimulative applications in repairs of various musculoskeletal tissues. It has been found that the periosteum contains mesenchymal progenitor cells capable of differentiating into either osteoblasts or chondrocytes depending on the culture conditions. Anatomically, the periosteum is a heterogeneous multi-layered membrane, consisting of an inner cambium and an outer fibrous layer. The present study was designed to elucidate the cellular phenotypic characteristics of cambium and fibrous layer cells in vitro, and to assess whether structural integrity of the tendon in the bone tunnel can be improved by periosteal augmentation of the tendon­bone interface. It was found the cells from each layer showed distinct phenotypic characteristics in a primary monolayer culture system. Specifically, the cambium cells demonstrated higher osteogenic characteristics (higher alkaline phosphatase and osteocalcin levels), as compared to the fibrous cells. Also in vivo animal model showed that a periosteal augmentation of a tendon graft could enhance the structural integrity of the tendon-bone interface, when the periosteum is placed between the tendon and bone interface with the cambium layer facing toward the bone. These findings suggest that extra care needs to be taken in order to identify and maintain the intrinsic phenotypes of the heterogeneous cell types within the periosteum. This will improve our understanding of periosteum in applications for musculoskeletal tissue repairs and tissue engineering.
Keywords
Osteogenic Potential; Bone Healing; Periosteum; Augmentation;
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1 F.E. Blaisdell, 'The osteogenetic function of the periosteum', Arch. Surg., Vol. 11, pp.933, 1925
2 P. Reynders, J. Becker, P. Broos, 'Osteogenic ability of free periosteal autografts in tibial fractures with severe soft tissue damage: an experimetal study', J. Orthop. Trauma, Vol. 13. No.2, pp.121-128, 1999   DOI   ScienceOn
3 A. Takushima, Y. Kitano, K. Harii, 'Osteogenic potential of cultured periosteal cells in a distracted bone gap in rabbits', J. Surg. Res., Vol. 78, pp.68-77, 1998   DOI   ScienceOn
4 N. Isogai, W.J. Landis, R. Mori, Y. Gotoh, L.C. Gerstenfeld, J. Upton, J.P. Vacanti, 'Experimental use of fibrin glue to induce site-directed osteogenesis from cultured periosteal cells', Plastic & Reconst. Surgery, Vol. 105, No.3, pp.953-963, 2000   DOI   ScienceOn
5 S.W. O'Driscoll, F.W. Keeley, R.B. Salter, 'The chondrogenic potential of free autogenous periosteal grafts for biological resurfacing of major full-thickness defects in joint surfaces under the influence of continuous passive motion. An experimental investigation in the rabbit', J Bone Joint Surg Am, Vol. 68, No.7, pp.1017-35, 1986
6 Y. Koshihara, M. Kawamura, S. Endo, C. Tsutsumi, H. Kodama, H. Oda, S. Higaki, 'Establishment of human osteoblastic cells derived from periosteum in culture', In Vitro Cell Dev Biol, Vol. 25, No.1, pp.37-43, 1989   DOI
7 M. Poussa, V. Ritsila, 'The osteogenic capadty of free periosteal and osteoperiosteal grafts. A comparative study in growing rabbits', Acta Orthop Scand, Vol. 50, No.5, pp.491-499, 1979
8 R. Gruber, C. Mayer, K. Bobacz, M.T. Krauth, W. Graninger, F.P. Luyten, L. Erlacher, 'Effects of cartilage-derived morphogenetic proteins and osteogenic protein-L on osteochondrogenic differentiation of periosteum-derived cells', Endocrinology, Vol. 142, No.5, pp.2087-94, 2001   DOI   ScienceOn
9 C.T. Brighton, J.R. Fisher, Jr., S.E. Levine, J.R. Corsetti, T. Reilly, A.S. Landsman, J.L. Williams, L.E. Thibault, 'The biochemical pathway mediating the proliferative response of bone cells to a mechanical stimulus', J. Bone Joint Surg Am, Vol. 78, No.9, pp.1337-47, 1996
10 M. Letts, E. Pang, J. Yang, B. Carpenter, 'Periosteal augmentation of the acetabulum', Clin. Orthop. Rel. Res., Vol. 354, pp.216-223, 1998   DOI   PUBMED
11 E.A. Tonna, E.P. Cronkite, 'The periosteum. Autoradiographic studies on cellular proliferation and transformation utilizing tritiated thymidine', Clin Orthop, Vol. 30, pp.218-33, 1963
12 S. Bahrami, U. Stratmann, H.P. Wiesmann, K. Mokrys, P. Bruckner, T. Szuwart, 'Periosteally derived osteoblastlike cells differentiate into chondrocytes in suspension culture in agarose', Anat Rec, Vol. 259, No.2, pp.124-30, 2000   DOI   ScienceOn
13 N. Isogai, W. Landis, T.H. Kim, L.C. Gerstenfeld, J. Upton, J.P. Vacanti, 'Formation of phalanges and small joints by tissue-engineering', J. Bone Jt. Surg., Vol. 81-A, No.3, pp.306-316, 1999
14 S.H. Liu, V. Panossian, R. al-Shaikh, E. Tomin, E. Shepherd, G.A. Finerman, J.M. Lane, 'Morphology and matrix composition during early tendon to bone healing', Clin Orthop, Vol. 339, pp.253-260, 1997   DOI   PUBMED
15 V.E. Hoikka, H.J. Jaroma, V.A. Ritsila, 'Reconstruction of the patellar articulation with periosteal grafts. 4- year follow-up of 13 cases', Acta Orthop Scand, Vol. 61, No.1, pp.36-9, 1990
16 S. Nehrer, M. Spector, T. Minas, 'Histologic analysis of tissue after failed cartilage repair procedures', Clin. Orthop. Rel. Res., Vol. 365, pp.149-162, 1999   DOI   PUBMED
17 J.A. Deren, F.S. Kaplan, C.T. Brighton, 'Alkaline phosphatase production by periosteal cells at various oxygen tensions in vitro', Clin Orthop, Vol. 252, pp.307-12, 1990
18 S.W. O'Driscoll, D.B. Saris, Y. Ito, J.S. Fitzimmons, 'The chondrogenic potential of periosteum decreases with age', J. Orthop Res., Vol. 19, No.1, pp.95-l03, 2001
19 A.S. Breitbart, D.A. Grande, J.M. Mason, M. Barcia, T. James, R.T. Grant, 'Gene-enhanced tissue engineering: app.lications for bone healing using cultured periosteal cells transduced retrovirally with the BMP-7 gene', Ann. Plastic Surg., Vol. 42, No.5, pp.488-495, 1999
20 .H. Wlodarski, 'Normal and heterotopic periosteum', Clin Orthop, Vol. 241, pp.265-77, 1989
21 Y. Ito, A. Sanyal, J.S. Fitzsimmons, M.A. Mello, S.W. O'Driscoll, 'Histomorphological and proliferative characterization of developing periosteal neochondrocytes in vitro', J Orthop Res, Vol. 19, No.3, pp.405-13, 2001   DOI   ScienceOn
22 E.H. Burger, P.M. Boonekamp, P.J. Nijweide, 'Osteoblast and osteoclast precursors in primary cultures of calvarial bone cells', Anat Rec, Vol. 214, No.1, pp.32-40., 1986   DOI   ScienceOn
23 S.A. Rodeo, K. Suzuki, X. Deng, J. Wozney, R Warren, 'Use of recombinant human bone morphogenetic protein-2 to enhance tendon healing in a bone tunnel', Am J Sports Med, Vol. 27, No.4, pp.476-488, 1999
24 S.W. O'Driscoll, J.S. Fitzsimmons, 'The importance of procedure specific training in harvesting periosteum for chondrogenesis', Clin. Orthop. Rel. Res., Vol. 380, pp.269-278, 2000   DOI   ScienceOn
25 T. Izumi, S.P. Scully, A. Heydemann, M.E. Bolander, 'Transforming growth factor beta 1 stimulates type II collagen expression in cultured periosteum-derived cells', J. Bone Miner Res., Vol. 7, No.1, pp.115-21, 1992
26 H. Nakahara, S.P. Bruder, V.M. Goldberg, A.I. Caplan, 'In vivo osteochondrogenic potential of cultured cells derived from the periosteum', Clin Orthop, Vol. 259, pp.223-32, 1990
27 S. Wakitani, T. Goto, S.J. Pineda, R.G. Young, Mansour.J.M., A. I. Caplan, V.M. Goldberg, 'Mesenchymal cell based repair of large, full-thickness defects of articular cartilage', J. Bone Jt. Surg., Vol. 76A, pp.579-592, 1994
28 K. Anderson, A.M. Seneviratne, K. Izawa, B.L. Atkinson, H.G. Potter, S.A. Rodeo, 'Augmentation of tendon healing in an intraarticular bone tunnel with use of a bone growth factor', Am J. Sports Med., Vol. 29, No.6, pp.689-698, 2001
29 R Ghilzon, C.A. McCulloch, R Zohar, 'Stromal mesenchymal progenitor cells'. Leuk Lymphoma, Vol. 32, No. 3-4, pp.211-221, 1999   DOI   PUBMED
30 R.C. Thomson, A.G. Mikos, E. Beahm, J.C. Lemon, W.C. Satterfield, T.B. Aufdemorte, M.J. Miller, 'Guided tissue fabrication from periosteum using preformed biodegradable polymer scaffolds', Biomaterials, Vol. 20, No.21, pp.2007-2018, 1999
31 T. Ueno, T. Kagawa, N. Mizukawa, H. Nakamura, T. Sugahara, T. Yamamoto, 'Cellular origin of endochondral ossification from grafted periosteum', Anat Rec, Vol. 264, No.4, pp.348-57, 2001   DOI   ScienceOn
32 H. Nakahara, V.M. Goldberg, A.I. Caplan, 'Cultureexpanded human periosteal-derived cells exhibit osteochondral potential in vivo', J Orthop Res., Vol. 9, pp.465- 476, 1991   DOI
33 S.H. Gallay, Y. Miura, C.N. Commisso, J.S. Fitzsimmons, S.W. O'Driscoll, 'Relationship of donor site to chondrogenic potential of periosteum in vitro', J. Orthop Res, Vol. 12, No.4, pp.515-25, 1994   DOI   ScienceOn
34 T. Nishimura, D.J. Simmons, E.G. Mainous, 'The origin of bone formed by heterotopic periosteal autografts', J. Oral Maxillofac. Surg., Vol. 55, No.11, pp.1265-1268, 1997   DOI   ScienceOn
35 A.S. Breitbart, D.A. Grande, R Kessler, J.T. Ryaby, R.J. Fitzsimmons, R.T. Grant, 'Tissue engineered bone repair of calvarial defects using cultured periosteal cells', Plast. Recon. Surg., Vol. 101, No.3, pp.567-576, 1998   DOI   ScienceOn
36 O.L. Korkala, 'Periosteal primary resurfacing of joint surface defects of the patella due to injury', Injury, Vol. 19, No.3, pp.216-8, 1988   DOI   PUBMED   ScienceOn
37 M. Iwasaki, H. Nakahara, K. Nakata, T. Nakase, T. Kimura, K. Ono, 'Regulation of proliferation and osteochondrogenic differentiation of periosteum-derived cells by transforming growth factor-beta and basic fibroblast growth factor', J. Bone Jt. Surg., Vol. 77-A, No.4, pp.543-554, 1995