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Influence of Periosteum Location on the Bone and Cartilage in Tissue-Engineered Phalanx

Published:March 19, 2019DOI:https://doi.org/10.1016/j.jhsa.2019.02.002

      Purpose

      This study investigated the influence of periosteal tissue of different origins on the calcification at the diaphysis and chondrocyte maturation at the epiphysis in an engineered phalanx. We hypothesized that the periosteum from long bones would better provide donor cells for bone formation and signals for maturation of the joint cartilage.

      Methods

      Periosteum was harvested from 4 locations (cranium, mandible, radius, and ilium) of calf bones. A human phalangeal bone-shaped, biodegradable, 3-dimensional scaffold hydroxyapatite-poly L-lactic-ɛ-caprolactone (HA-P[LA/CL]) was prepared using a human phalangeal bone-shaped template. A bioengineered human phalanx was fabricated by combining periosteal grafts with biodegradable copolymers. The joint cartilage region (chondrocyte/polyglycolic acid [PGA] composite) was subsequently sutured to the phalangeal bone region (periosteum/HA-P[LA/CL] composite) with absorbable sutures to make a human phalangeal bone model. These were then implanted in nude mice for maturation of the constructs. Macroscopic, radiographic, histological, and immune-histochemical evaluations were carried out to determine the relative influence of the periosteal graft source on bone and cartilage formation at 10 and 20 weeks after implantation.

      Results

      Calcification localized under the periosteum was noted in the cranium, radius, and ilium groups after 10 weeks, which markedly expanded at the modelled diaphysis after 20 weeks. The width in the minor axis direction tended to increase with time after grafting in the cranium group, whereas the longitudinal length increased in the radius and ilium groups. The joint cartilage thickness changed with time depending on the type of periosteum, and periosteum collected from the radius and ilium was associated with the greatest cartilage thickness in the joint cartilage maturation process.

      Conclusions

      These results suggest that periosteum collected from radius of calves demonstrated superior bone formation and chondrocyte maturation in the engineered phalanx compared with other sources of periosteum.

      Clinical relevance

      The osteogenic capacity depends on the periosteal source regardless of intramembranous or endochondral ossification. The appropriate periosteal choice is essential in the phalangeal bone and cartilage tissue engineering. The results are important for broadening tissue engineering possibilities for clinical application.

      Key words

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      References

        • Hollinger J.O.
        • Brekke J.
        • Gruskin E.
        • Lee D.
        Role of bone substitutes.
        Clin Orthop Relat Res. 1996; 324: 55-65
        • Kitsugi T.
        • Yamamuro T.
        • Nakamura T.
        • Kotani S.
        • Kokubo T.
        • Takeuchi H.
        Four calcium phosphate ceramics as bone substitutes for non–weight-bearing.
        Biomaterials. 1993; 14: 216-224
        • Malizos K.N.
        • Papatheodorou L.K.
        The healing potential of the periosteum molecular aspects.
        Injury. 2005; 36: S13-S19
        • Stevens M.M.
        • Marini R.P.
        • Schaefer D.
        • Aronson J.
        • Langer R.
        • Shastri V.P.
        In vivo engineering of organs: the bone bioreactor.
        Proc Natl Acad Sci U S A. 2005; 102: 11450-11455
        • Isogai N.
        • Landis W.
        • Kim T.H.
        • Gerstenfeld L.C.
        • Upton J.
        • Vacanti J.P.
        Formation of phalanges and small joints by tissue engineering.
        J Bone Joint Surg Am. 1999; 81: 306-316
        • Isogai N.
        • Landis W.
        Phalanges and small joints.
        in: Atla A. Lanza R. Methods of Tissue Engineering. San Diego Academic Press, San Diego2001: 1041-1047
        • Chubinskaya S.
        • Jacquet R.
        • Isogai N.
        • Asamura S.
        • Landis W.J.
        Characterization of the cellular origin of a tissue-engineered human phalanx model by in situ hybridization.
        Tissue Eng. 2004; 10: 1204-1213
        • Landis W.J.
        • Jacquet R.
        • Hillyer J.
        • et al.
        The potential of tissue engineering in orthopedics.
        Orthop Clin North Am. 2005; 36: 97-104
        • Potter K.
        • Sweet D.E.
        • Anderson P.
        • et al.
        Non-destructive studies of tissue-engineered phalanges by magnetic resonance microscopy and X-ray microtomography.
        Bone. 2006; 38: 350-358
        • Isogai N.
        • Tokui T.
        Finger regeneration using an osteo-inductive biodegradable poly (L-lactide-caprolactone) copolymer with hydroxyapatit.
        in: Comprehensive Biomaterials. Vol. 5. Elsevier, Oxford, UK2011: 541-546
        • Matsushima S.
        • Isogai N.
        • Jacquet R.
        • Lowder E.
        • Tokui T.
        • Landis W.J.
        The nature and role of periosteum in bone and cartilage regeneration.
        Cells Tissues Organs. 2011; 194: 320-325
        • Klagsbrun M.
        Large-scale preparation of chondrocytes.
        Methods Enzymol. 1979; 58: 560-564
        • Asamura S.
        • Ikada Y.
        • Matsunaga K.
        • et al.
        Treatment of orbital floor fracture using a periosteum-polymer complex.
        J Craniomaxillofac Surg. 2010; 38: 197-203
        • O'Driscoll S.W.
        • Fitzsimmons J.S.
        The role of periosteum in cartilage repair.
        Clin Orthop Relat Res. 2001; 391: S190-S207
        • Szulc P.
        • Seeman E.
        • Duboeuf F.
        • Sornay-Rendu E.
        • Delmas P.D.
        Bone fragility: failure of periosteal apposition to compensate for increased endocortical resorption in postmenopausal women.
        J Bone Miner Res. 2006; 21: 1856-1863
        • Gallay S.H.
        • Miura Y.
        • Commisso C.N.
        • Fitzsimmons J.S.
        • O’Driscoll S.W.
        Relationship of donor site to chondrogenic potential of periosteum in vitro.
        J Orthop Res. 1994; 12: 515-525
        • Nakahara H.
        • Dennis J.E.
        • Bruder S.P.
        • Haynesworth S.E.
        • Lennon D.P.
        • Caplan A.I.
        In vitro differentiation of bone and hypertrophic cartilage from periosteal-derived cells.
        Exp Cell Res. 1991; 195: 492-503
        • Nakahara H.
        • Bruder S.P.
        • Goldberg V.M.
        • Caplan A.I.
        In vivo osteochondrogenic potential of cultures cells derived from the periosteum.
        Clin Orthop Relat Res. 1990; 259: 223-232
        • Nakahara H.
        • Goldberg V.M.
        • Caplan A.I.
        Culture-expanded periosteal-derived cells exhibit osteochondrogenic potential in porous calcium phosphate ceramics in vivo.
        Clin Orthop Relat Res. 1992; 276: 291-298
        • Iwasaki M.
        • Nakahara H.
        • Nakata K.
        • Nakase T.
        • Kimura T.
        • Ono K.
        Regulation of proliferation and osteochondrogenic differentiation of periosteum-derived cells by transforming growth factor-beta and basic fibroblast growth factor.
        J Bone Joint Surg Am. 1995; 7: 543-554
        • Iwasaki M.
        • Nakahara H.
        • Nakase T.
        • et al.
        Bone morphogenetic protein 2 stimulates osteogenesis but does not affect chondrogenesis in osteochondrogenic differentiation of periosteum-derived cells.
        J Bone Miner Res. 1994; 9: 1195-1204
        • Jiang X.
        • Iseki S.
        • Maxson R.E.
        • Sucov H.M.
        • Morriss-Kay G.M.
        Tissue origins and interactions in the mammalian skull vault.
        Dev Biol. 2002; 241: 106-116
        • Di Rocco F.
        • Biosse Duplan M.
        • Heuzé Y.
        • et al.
        FGFR3 mutation causes abnormal membranous ossification in achondroplasia.
        Hum Mol Genet. 2014; 23: 2914-2925
        • Mundlos S.
        • Otto F.
        • Mundios C.
        • et al.
        Mutations involving the transcriptional factor CBFA 1 cause cleidocranial dysplasia.
        Cell. 1997; 89: 773-779
        • Favus M.J.
        Primer on the Metabolic Bone Diseases and Disorders of Mineral Metabolism.
        3th ed. Lippincott-Raven, New York1996: 3
        • Fan W.
        • Crawford R.
        • Xiao Y.
        Structural and cellular differences between metaphyseal and diaphyseal periosteum in different aged rats.
        Bone. 2008; 42: 81-89
        • Alvarez J.
        • Horton J.
        • Sohn P.
        • Serra R.
        The perichondrium plays an important role in mediating the effects of TGF-beta1 on endochondral bone formation.
        Dev Dyn. 2001; 221: 311-321
        • Faucheux C.
        • Nicholls B.M.
        • Allen S.
        • Danks J.A.
        • Horton M.A.
        • Price J.S.
        Recapitulation of the parathyroid hormone-related peptide-Indian hedgehog pathway in regenerating deer antler.
        Dev Dyn. 2004; 231: 88-97
        • Bandyopadhyay A.
        • Kubilus J.K.
        • Crochiere M.L.
        • Linsenmayer T.F.
        • Tabin C.J.
        Identification of unique molecular subdomains in the perichondrium and periosteum and their role in regulating gene expression in the underlying chondrocytes.
        Dev Biol. 2008; 321: 162-174
        • Goldring M.B.
        • Tsuchimochi K.
        • Ijiri K.
        The control of chondrogenesis.
        J Cell Biochem. 2006; 97: 33-44
        • de Crombrugghe B.
        • Lefebvre V.
        • Nakashima K.
        Regulatory mechanisms in the pathways of cartilage and bone formation.
        Curr Opin Cell Biol. 2001; 13: 721-727
        • Kronenberg H.M.
        Developmental regulation of the growth plate.
        Nature. 2003; 423: 332-336
        • Provot S.
        • Schipani E.
        Molecular mechanisms of endochondral bone development.
        Biochem Biophys Res Commun. 2005; 328: 658-665
        • Eames B.F.
        • de la Fuente L.
        • Helms J.A.
        Molecular ontogeny of the skeleton.
        Birth Defects Res C Embyo Today. 2003; 69: 93-101
        • Ballock R.T.
        • O’Keefe R.J.
        The biology of the growth plate.
        J Bone Joint Surg Am. 2003; 85-A: 715-726