Download PDF
Indian J Plast Surg 2008; 41(01): 38-46
DOI: 10.1055/s-0039-1699225
Invited Article
Association of Plastic Surgeons of India

Tissue engineering approaches for the construction of a completely autologous tendon substitute

Bassetto Franco
Clinic of Plastic Surgery, Department of Medical and Surgical Specialities
,
Vindigni Vincenzo
Clinic of Plastic Surgery, Department of Medical and Surgical Specialities
,
Dalla Vedova Alessandro
Clinic of Plastic Surgery, Department of Medical and Surgical Specialities
,
Carolin Tonello
1   Department of Histology, Microbiology and Medical Biotechnology, University of Padova, Padova, Italy
,
Giovanni Abatangelo
1   Department of Histology, Microbiology and Medical Biotechnology, University of Padova, Padova, Italy
,
Francesco Mazzoleni
› Author Affiliations
Further Information

Publication History

Publication Date:
15 January 2020 (online)

Also available at
  PDF Download Permissions and Reprints

ABSTRACT

Tissue engineering is a multidisciplinary field that involves the application of the principles and methods of engineering and life sciences towards i) the fundamental understanding of structure-function relationships in normal and pathological mammalian tissues and ii) the development of biological substitutes that restore, maintain or improve tissue function. The goal of tissue engineering is to surpass the limitations of conventional treatments based on organ transplantation and biomaterial implantation. The field of tendon tissue engineering is relatively unexplored due to the difficulty in in vitro preservation of tenocyte phenotype. Only recently has mechanobiology allowed us to gain a better understanding of the fundamental role of in vitro mechanical stimuli in maintaining the phenotype of tendinous tissue. This review analyzes the techniques used so far for in vitro regeneration of tendinous tissue.

KEYWORDS

Biomaterials - bioreactor - mechanobiology - tendon - tissue engineering
 
  • 1 Louie L, Yannas I, Spector M. Tissue engineered tendon. In: Patrick Jr C, Mikos A, McIntire L. editors. Frontiers in tissue engineering.. New York: Elsevier Science Ltd; 1998: p.413-42
    Google Scholar
  • 2 Woo SL, Abramowitch SD, Kilger R, Liang R. Biomechanics of knee ligaments: Injury, healing, and repair. J Biomech 2006; 39: 1-20
    CrossrefPubMedGoogle Scholar
  • 3 Kim CW, Pedowitz RA. Part A: Graft choices and the biology of graft healing. Daniel′s Knee Injuries 2003; p.435-91
    Google Scholar
  • 4 Goulet F, Rancourt D, Cloutier R, Germain L, Poole A, Auger F. Tendons and ligaments. Principles of tissue engineering 2000; p.711-22
    Google Scholar
  • 5 Doroski DM, Brink KS, Johnna S. Techniques for biological characterization of tissue-engineered tendon and ligament. Biomaterials 2007; 28: 187-202
    CrossrefPubMedGoogle Scholar
  • 6 Butler D, Awad H. Perspectives on cell and collagen composites for tendon repair. Clin Orthop Relat Res 1999; 367: 324-32
    CrossrefPubMedGoogle Scholar
  • 7 Henshaw D, Attia E, Bhargava E, Hannafin J. Canine AC. Fibroblast integrin expression and cell alignment in response to cyclic tensile strain in three-dimensional collagen gels. J Orthop Res 2006; 24: 481-90
    CrossrefPubMedGoogle Scholar
  • 8 Musahl V, Abramowitch S, Gilbert T, Tsuda E, Wang J, Badylak S. et.al. The use of porcine small intestinal submucosa to enhance the healing of the medial collateral ligament a functional tissue engineering study in rabbits. J Orthop Res 2004; 22: 214-20
    CrossrefPubMedGoogle Scholar
  • 9 Rodeo SA, Maher SA, Hidaka C. What′s new in orthopaedic research. J Bone J Surg Am 2004; 86: 2085-95
    Google Scholar
  • 10 Funakoshi T, Majima T, Iwasaki N, Suenaga N, Sawaguchi N, Shimode K. et.al. Application of tissue engineering techniques for rotator cuff regeneration using a chitosan-based hyaluronan hybrid fiber scaffold. Am J Sports Med 2005; 33: 1193-201
    CrossrefPubMedGoogle Scholar
  • 11 Majima T, Funakosi T, Iwasaki N, Yamane ST, Harada K, Nonaka S. et.al. Alginate and chitosan polyion complex hybrid fibers for scaffolds in ligament and tendon tissue engineering. J Orthop Sci 2005; 10: 302-7
    CrossrefPubMedGoogle Scholar
  • 12 Funakoshi T, Majima T, Iwasaki N, Suenaga N, Sawaguchi N, Shimode K. et.al. Application of tissue engineering techniques for rotator cuff regeneration using a chitosan-based hyaluronan hybrid fiber scaffold. Am J Sports Med 2005; 33: 1193-201
    CrossrefPubMedGoogle Scholar
  • 13 Altman GH, Horan RL, Lu HH, Moreau J, Martin I, Richmond JC. et.al. Silk matrix for tissue engineered anterior cruciate ligaments. Biomaterials 2002; 23: 4131-41
    CrossrefPubMedGoogle Scholar
  • 14 Chen J, Altman GH, Karageorgiou V, Horan R, Collette A, Volloch V. et.al. Human bone marrow stromal cell and ligament fibroblast responses on RGD-modified silk fibers. J Biomed Mater Res A 2003; 67: 559-70
    PubMedGoogle Scholar
  • 15 Altman GH, Diaz F, Jakuba C, Calabro T, Horan RL, Chen J. et.al. Silk-based biomaterials. Biomaterials 2003; 24: 401-16
    CrossrefPubMedGoogle Scholar
  • 16 Martinek V, Latterman C, Usas A, Abramowitch S, Woo SL, Fu FH. et.al. Enhancement of tendon-bone integration of anterior cruciate ligament grafts with bone morphogenetic protein-2 gene transfer: A histological and biomechanical study. J Bone J Surg Am 2002; 84: 1123-31
    Google Scholar
  • 17 Ahmed Z, Underwood S, Brown RA. Low concentrations of fibrinogen increase cell migration speed on fibronectin/fibrinogen composite cables. Cell Motil Cytoskeleton 2000; 46: 6-16
    CrossrefPubMedGoogle Scholar
  • 18 Lu HH, Cooper JA, Manuel S, Freeman JW, Attawia MA, Ko FK. et.al. Anterior cruciate ligament regeneration using braided biodegradable scaffolds:In vitro optimization studies. Biomaterials 2005; 26: 4805-16
    CrossrefPubMedGoogle Scholar
  • 19 Vunjak-Novakovic G, Altman G, Horan R, Kaplan DL. Tissue engineering of ligaments. Annu Rev Biomed Eng 2004; 6: 131-56
    CrossrefPubMedGoogle Scholar
  • 20 Ide A, Sakane M, Chen G, Shimojo H, Ushida T, Tateishi T. et.al. Collagen hybridization with poly(L-lactic acid) braid promotes ligament cell migration. Mater Sci Eng C 2001; C17: 95-9
    CrossrefGoogle Scholar
  • 21 Cooper JA, Lu HH, Ko FK, Freeman JW, Laurencin CT. Fiberbased tissue-engineered scaffold for ligament replacement: Design considerations and in vitro evaluation. Biomaterials 2004; 26: 1523-32
    Google Scholar
  • 22 Qin TW, Yang ZM, Wu ZZ, Xie HQ, Qin J, Cai SX. Adhesion strength of human tenocytes to extracellular matrix componentmodified poly(DL-lactide-co-glycolide) substrates. Biomaterials 2005; 26: 6635-42
    CrossrefPubMedGoogle Scholar
  • 23 Auger FA, Rouabhia M, Goulet F, Berthod F, Moulin V, Germain L. Tissue-engineered human skin substitutes developed from collagen-populated hydrated gels: Clinical and fundamental. Med Biol Eng Comput 1998; 6: 801-12
    Google Scholar
  • 24 Huang D, Chang TR, Aggarwal A, Lee RC, Ehrlich HP. Mechanisms and dynamics of mechanical strengthening in ligament-equivalent fibroblast-populated collagen matrices. Ann Biomed Eng 1993; 3: 289-305
    Google Scholar
  • 25 Bell E, Ivarsson B, Merrill C. Production of a tissue-like structure by contraction of collagen lattices by human fibroblasts of different proliferative potential in vitro. Proc Nat Acad Sci USA 1979; 3: 1274-8
    Google Scholar
  • 26 Klebe RJ, Caldwell H, Milam S. Cells transmit spatial information by orienting collagen fibers. Matrix 1989; 6: 451-8
    Google Scholar
  • 27 Nishiyama T, Tsunenaga M, Akutsu N, Horii I, Nakayama Y, Adac E. et.al. Dissociation of actin microfilament organization from acquisition and maintenance of elongated shape of human dermal fibroblasts in three-dimensional collagen gel. Matrix 1993; 6: 447-55
    Google Scholar
  • 28 Ben-Zeev A, Farmer SR, Penman S. Protein synthesis requires cell-surface contact while nuclear events respond to cell shape in anchorage-dependent fibroblasts. Cell 1980; 2: 365-72
    Google Scholar
  • 29 Kurtz J, Harris AK, Stopak D, Wild P. Fibroblast traction as a mechanism for collagen morphogenesis. Nature 1981; 290: 249-51
    CrossrefPubMedGoogle Scholar
  • 30 Maciera-Coelho A, Garcia-Giralt E, Adrian M. Changes in lysosomal associated structures in human fibroblasts kept in resting phase. Proc Soc Exp Biol Med 1971; 2:: 712-8
    Google Scholar
  • 31 Bellincampi LD, Closkey RF, Prasad R, Zawadsky JP, Dunn M. Viability of fibroblast-seeded ligament analogs after autogenous implantation. J Orthop Res 1998; 4: 414-20
    Google Scholar
  • 32 Dunn MG, Liesch JB, Tiku ML, Zawadsky JP. Development of fibroblast-seeded ligament analogs for ACL reconstruction. J Biomed Mater Res 1995; 11: 1363-71
    Google Scholar
  • 33 Brody GA, Eisinger M, Arnoczky SP, Warren RF. In vitro fibroblast seeding of prosthetic anterior cruciate ligaments: A preliminary study. Am J Sports Med 1988; 3: 203-8
    Google Scholar
  • 34 Athanasiou KA, Niederauer GG, Agrawal CM. Sterilization, toxicity, biocompatibility and clinical applications of polylactic acid/polyglycolic acid copolymers. Biomaterials 1996; 2: 93-102
    Google Scholar
  • 35 Ghersi R, Cavallaro AM, Lodi V, Missere M, Violante FS. Repetitive movement of the upper limbs: Results of a current exposure evaluation and a clinical investigation in workers employed in the preparation of pork meat in the province of Modena. Med Lav 1996; 6: 656-74
    Google Scholar
  • 36 Chvapil M, Speer DP, Holubec H, Chvapil TA, King DH. Collagen fibers as a temporary scaffold for replacement of ACL in goats. J Biomed Mater Res 1993; 3: 313-25
    Google Scholar
  • 37 Infeld MD, Brennan JA, Davis PB. Human tracheobronchial epithelial cells direct migration of lung fibroblasts in three-dimensional collagen gels. Am J Physiol 1992; 5 L 535-41
    Google Scholar
  • 38 Gentleman E, Lay AN, Dickerson DA, Nauman EA, Livesay GA, Dee KC. Mechanical characterization of collagen fibers and scaffolds for tissue engineering. Biomaterials 2003; 21: 3805-13
    Google Scholar
  • 39 Sato M, Maeda M, Kurosawa H, Inoue Y, Yamauchi Y, Iwase H. Reconstruction of rabbit Achilles tendon with three bioabsorbable materials: Histological and biomechanical studies. J Orthop Sci 2000; 3: 256-67
    Google Scholar
  • 40 Wasserman AJ, Kato YP, Christiansen D, Dunn MG, Silver FH. Achilles tendon replacement by a collagen fiber prosthesis: Morphological evaluation of neotendon formation. Scanning Microsc 1989; 3: 1183-97
    PubMedGoogle Scholar
  • 41 Laurencin CT, Ambrosio AM, Borden MD, Cooper Jr JA. Tissue engineering: Orthopedic applications. Annu Rev Biomed Eng 1999; 1: 19-46
    CrossrefPubMedGoogle Scholar
  • 42 Kisiday JD, Jin M, DiMicco MA, Kurz B, Grodzinsky AJ. Effects of dynamic compressive loading on chondrocyte biosynthesis in self-assembling peptide scaffolds. J Biomech 2004; 5: 595-604
    Google Scholar
  • 43 Altman G, Horan R, Martin I, Farhadi J, Stark P, Volloch V. et.al. Cell differentiation by mechanical stress. FASEBJ 2002; 16: 270-2
    CrossrefPubMedGoogle Scholar
  • 44 Musahl V, Abramowitch SD, Gilbert TW, Tsuda E, Wang JH, Badylak SF. The use of porcine small intestinal submucosa to enhance the healing of the medial collateral ligament a functional tissue engineering study in rabbits. J Orthop Res 2004; 1: 214-20
    Google Scholar
  • 45 Li F, Li B, Wang QM, Wang JH. Cell shape regulates collagen type I expression in human tendon fibroblasts. Cell Motil Cytoskeleton 2008; 31: 1-10
    Google Scholar
  • 46 Bagnaninchi PO, Yang Y, El Hai AJ, Maffulli N. Tissue engineering for tendon repair. Br J Sports Med 2007; 41: e10
    CrossrefPubMedGoogle Scholar
  • 47 Yao L, Bestwick CS, Bestwick LA, Maffulli N, Aspden RM. Phenotipic drift in human tenocyte culture. wTissue Eng 2006; 12: 1843-9
    Google Scholar
  • 48 Cao D, Liu W, Wei X, Xu F, Cui L, Cao Y. In vitro tendon engineering with avian tenocytes and poliglicolic acids: A preliminary report. Tissue Eng 2006; 12: 1369-77
    CrossrefPubMedGoogle Scholar
  • 49 Awad HA, Butler DL, Boivin GP, Smith FN, Malaviya P, Huibregtse B. et.al. Autologous mesenchimal stem cell-mediated repair of tendon. Tissue Eng 1999; 5: 267-77
    CrossrefPubMedGoogle Scholar
  • 50 Awad HA, Butler DL, Harris MT, Ibrahim RE, Wu Y, Young RG. et.al. In vitro characterization of mesencymal stem cell-seeded collagen scaffolds for tendon repair: Effects of initial seeding density on contraction kinetics. J Biomed Mater Res 2000; 51: 233-40
    CrossrefPubMedGoogle Scholar
  • 51 Ge Z, Gohm J, Lee E. Selection of cell source for ligament tissue engineering. Cell Transplant 2005; 14: 573-83
    CrossrefPubMedGoogle Scholar
  • 52 Kall S, Nath U, Reimers K, Choi CY, Muehlberger T, Allmeling C. et.al. In vitro fabrication of tendon substitutes using human mesenchymal stem cells and a collagen type I gel. Handchir Mikrochir Plast Chir 2004; 36: 205-11
    Article in Thieme ConnectPubMedGoogle Scholar
  • 53 Kryger GS, Chong AK, Costa M, Pham H, Bates SJ, Chang J. A comparison of tenocytes and mesenchymal stem cells for use in flexor tendon tissue engineering. J Hand Surg 2007; 32: 597-605
    CrossrefPubMedGoogle Scholar
  • 54 Wolfman NM, Hattersley G, Cox K, Celeste AJ, Nelson R, Yamaji N. et.al. Ectopic induction of tendon and ligament in rats by growth and differentiation factors 5 6 and 7, members of the TGF-beta gene family. J Clin Invest 1997; 100: 321-30
    CrossrefPubMedGoogle Scholar
  • 55 Hoffmann A, Gross G. Tendon and ligament engineering: From cell biology to in vivo application. Regen Med 2006; 1: 563-74
    CrossrefPubMedGoogle Scholar
  • 56 Chan BP, Fu S, Qin L, Lee K, Rolf CG, Chan K. Effects of basic fibroblast growth factor (bFGF) on early stages of tendon healing: A rat patellar tendon model. Acta Orthop Scand 2000; 71: 513-8
    CrossrefPubMedGoogle Scholar
  • 57 Hildebrand KA, Woo SL, Smith DW, Allen CR, Deie M, Taylor BJ. et.al. The effects of platelet-derived growth factor-BB on healing of the rabbit medial collateral ligament: An in vivo study. Am J Sports Med 1998; 26: 549-54
    CrossrefPubMedGoogle Scholar
  • 58 Batten ML, Hansen JC, Dahners LE. Influence of dosage and timing of application of platelet-derived growth factor on early healing of the rat medial collateral ligament. J Orthop Res 1996; 14: 736-41
    CrossrefPubMedGoogle Scholar
  • 59 Schmidt CC, Georgescu HI, Kwoh CK, Blomstrom GL, Engle CP, Larkin LA. et.al. Effect of growth factors on the proliferation of fibroblasts from the medial collateral and anterior cruciate ligaments. J Orthop Res 1995; 13: 184-90
    CrossrefPubMedGoogle Scholar
  • 60 Kurtz CA, Loebig TG, Anderson DD, DeMeo PJ, Campbell PG. Insulin-like growth factor I accelerates functional recovery from Achilles tendon injury in a rat model. Am J Sports Med 1999; 27: 363-9
    CrossrefPubMedGoogle Scholar
  • 61 D′Souza D, Patel K. Involvement of long and short-range signalling during early tendon development. Anat Embryol (Berl) 1999; 200: 367-75
    CrossrefPubMedGoogle Scholar
  • 62 Storm EE, Huynh TV, Copeland NG, Jenkins NA, Kingsley DM, Lee SJ. Limb alterations in brachypodism mice due to mutations in a new member of the TGF-β-superfamily. Nature 1994; 368: 639-43
    CrossrefPubMedGoogle Scholar
  • 63 Settle Jr SH, Rountree RB, Sinha A, Thacker A, Higgins K, Kingsley DM. Multiple joint and skeletal patterning defects caused by single and double mutations in the mouse Gdf6 and Gdf5 genes. Dev Biol 2003; 254: 116-30
    CrossrefPubMedGoogle Scholar
  • 64 Chhabra A, Tsou D, Clark RT, Gaschen V, Hunziker EB, Mikic B. GDF-5 deficiency in mice delays Achille′s tendon healing. J Orthop Res 2003; 21: 826-35
    CrossrefPubMedGoogle Scholar
  • 65 Mikic B, Schalet BJ, Clark RT, Gaschen V, Hunziker EB. GDF-5 deficiency in mice alters the ultrastructure, mechanic al properties and composition of the Achilles tendon. J Orthop Res 2001; 19: 365-71
    CrossrefPubMedGoogle Scholar
  • 66 Wolfman NM, Hattersley G, Cox K, Celeste AJ, Nelson R, Yamaji N. et.al. Ectopic induction of tendon and ligament in rats by growth and differentiation factors 5, 6, and 7, members of the TGF-β gene family. J Clin Invest 1997; 100: 321-30
    CrossrefPubMedGoogle Scholar
  • 67 Forslund C, Rueger D, Aspenberg P. A comparative dose-response study of cartilage-derived morphogenetic protein (CDMP)-1, -2 and -3 for tendon healing in rats. J Orthop Res 2003; 21: 617-21
    CrossrefPubMedGoogle Scholar
  • 68 Virchenko O, Fahlgren A, Skoglund B, Aspenberg P. CDMP-2 injection improves early tendon healing in a rabbit model for surgical repair. Scand J Med Sci Sports 2005; 15: 260-4
    CrossrefPubMedGoogle Scholar
  • 69 Lou J, Tu Y, Burns M, Silva MJ, Manske P. BMP-12 gene transfer augmentation of lacerated tendon repair. J Orthop Res 2001; 19: 1199-202
    CrossrefPubMedGoogle Scholar
  • 70 Sharma P, Maffulli N. Tendon injury and tendinopathy: Healing and repair. J Bone Joint Surg Am 2005; 87: 187-202
    PubMedGoogle Scholar
  • 71 Nakamura N, Timmermann SA, Hart DA, Kaneda Y, Shrive NG, Shino K. et.al. A comparison of in vivo gene delivery methods for antisense therapy in ligament healing. Gene Ther 1998; 5: 1455-61
    Google Scholar
  • 72 Nakamura N, Shino K, Natsuume T, Horibe S, Matsumoto N, Kaneda Y. et.al. Early biological effect of in vivo gene transfer of platelet-derived growth factor (PDGF)-B into healing patellar ligament. Gene Ther 1998; 5: 1165-70
    Google Scholar
  • 73 Hannallah D, Peterson B, Lieberman JR, Fu FH, Huard J. Gene therapy in orthopaedic surgery. Instr Course Lect 2003; 52: 753-68
    PubMedGoogle Scholar
  • 74 Nakamura N, Horibe S, Matsumoto N, Tomita T, Natsuume T, Kaneda Y. et.al. Transient introduction of a foreign gene into healing rat patellar ligament. J Clin Invest 1996; 97: 226-31
    CrossrefPubMedGoogle Scholar
  • 75 Gerich TG, Kang R, Fu FH, Robbins PD, Evans CH. Gene transfer to the rabbit patellar tendon: Potential for genetic enhancement of tendon and ligament healing. Gene Ther 1996; 3: 1089-93
    Google Scholar
  • 76 Gerich TG, Kang R, Fu FH, Robbins PD, Evans CH. Gene transfer to the patellar tendon. Knee Surg Sports Traumatol Arthrosc 1997; 5: 118-23
    CrossrefPubMedGoogle Scholar
  • 77 Lou J, Kubota H, Hotokezaka S, Ludwig FJ, Manske PR. In vivo gene transfer and over-expression of focal adhesion kinase (pp125 FAK) mediated by recombinant adenovirus-induced tendon adhesion formation and epitenon cell change. J Orthop Res 1997; 15: 911-8
    CrossrefPubMedGoogle Scholar
  • 78 Wolfman NM, Celeste AJ, Cox K. Preliminary characterization of the biological activities of rh BMP-12. J Bone Miner Res 1995; 10: S148
    Google Scholar
  • 79 Fu SC, Wong YP, Chan BP, Pau HM, Cheuk YC, Lee KM. et.al. The roles of bone morphogenetic protein (BMP) 12 in stimulating the proliferation and matrix production of human patellar tendon fibroblasts. Life Sci 2003; 72: 2965-74
    CrossrefPubMedGoogle Scholar
  • 80 Lou J, Tu Y, Burns M, Silva MJ, Manske P. BMP-12 gene transfer augmentation of lacerated tendon repair. J Orthop Res 2001; 19: 1199-202
    CrossrefPubMedGoogle Scholar
  • 81 Nakamura N, Shino K, Natsuume T, Horibe S, Matsumoto N, Kaneda Y. et.al. Early biological effect of in vivo gene transfer of platelet-derived growth factor (PDGF)-B into healing patellar ligament. Gene Ther 1998; 5: 1165-70
    Google Scholar
  • 82 Marchant JK, Hahn RA, Linsenmayer TF, Birk DE. Reduction of type V collagen using a dominant-negative strategy alters the regulation of fibrillogenesis and results in the loss of corneal-specific fibril morphology. J Cell Biol 1996; 135: 1415-26
    CrossrefPubMedGoogle Scholar
  • 83 Adachi E, Hayashi T. In vitro formation of hybrid fibrils of type V collagen and type I collagen: Limited growth of type I collagen into thick fibrils by type V collagen. Connect Tissue Res 1986; 14: 257-66
    CrossrefPubMedGoogle Scholar
  • 84 Niyibizi C, Kavalkovich K, Yamaji T, Woo SL. Type V collagen is increased during rabbit medial collateral ligament healing. Knee Surg Sports Traumatol Arthrosc 2000; 8: 281-5
    CrossrefPubMedGoogle Scholar
  • 85 Shimomura T, Jia F, Niyibizi C, Woo SL. Antisense oligonucleotides reduce synthesis of procollagen alpha1 (V) chain in human patellar tendon fibroblasts: Potential application in healing ligaments and tendons. Connect Tissue Res 2003; 44: 167-72
    CrossrefPubMedGoogle Scholar
  • 86 Hart DA, Nakamura N, Marchuk L, Hiraoka H, Boorman R, Kaneda Y. et.al. Complexity of determining cause and effect in vivo after antisense gene therapy. Clin Orthop Relat Res 2000; 379: S242-51
    CrossrefPubMedGoogle Scholar
  • 87 Nakamura N, Timmermann SA, Hart DA, Kaneda Y, Shrive NG, Shino K. et.al. A comparison of in vivo gene delivery methods for antisense therapy in ligament healing. Gene Ther 1998; 5: 1455-61
    Google Scholar
  • 88 Nakamura N, Hart DA, Boorman RS, Kaneda Y, Shrive NG, Marchuk LL. et.al. Decorin antisense gene therapy improves functional healing of early rabbit ligament scar with enhanced collagen fibrillogenesis in vivo. J Orthop Res 2000; 18: 517-23
    CrossrefPubMedGoogle Scholar
  • 89 Ingber DE. Mechanical control of tissue morphogenesis during embryological development. Int J Dev Biol 2006; 50: 255-66
    CrossrefPubMedGoogle Scholar
  • 90 Barkhausen T, van Griensven M, Zeichen J, Bosch U. Modulation of cell functions of human tendon fibroblasts by different repetitive cyclic mechanical stress patterns. Exp Toxicol Pathol 2003; 55: 153-8
    CrossrefPubMedGoogle Scholar
  • 91 Brown RA, Prajapati R, McGrouther DA, Yannas IV, Eastwood M. Tensional homeostasis in dermal fibroblasts: Mechanical responses to mechanical loading in three-dimensional substrates. J Cell Physiol 1998; 175: 323-32
    CrossrefPubMedGoogle Scholar
  • 92 Wang JH, Yang G, Li Z, Shen W. Fibroblast responses to cyclic mechanical stretching depend on cell orientation to the stretching direction. J Biomech 2004; 37: 573-6
    CrossrefPubMedGoogle Scholar
  • 93 Schulze-Tanzil G, Mobasheri A, Clegg PD, Sendzik J, John T, Shakibaei M. Cultivation of human tenocytes in high-density culture. Histochem Cell Biol 2004; 122: 219-28
    CrossrefPubMedGoogle Scholar
  • 94 Kessler D, Dethlefsen S, Haase I, Plomann M, Hirche F, Krieg T. et.al. Fibroblasts in mechanically stressed collagen lattices assume a "synthetic" phenotype. J Biol Chem 2001; 276: 36575-85
    CrossrefPubMedGoogle Scholar
  • 95 Slutek M, Van GM, Zeichen J, Brauer N, Bosch U. Cyclic mechanical stretching modulates secretion pattern of growth factors in human tendon fibroblasts. Eur J Appl Physiol 2001; 86: 48-52
    CrossrefPubMedGoogle Scholar
  • 96 Zeichen J, Van GM, Bosch U. The proliferative response of isolated huaman tendon fibroblasts to cyclic biaxial mechanical strain. Am J Sport Med 2000; 28: 888-92
    CrossrefPubMedGoogle Scholar
  • 97 Yang G, Crawford RC, Wang JH. Proliferation and collagen production of human patellar tendon fibroblasts in response to cyclic uniaxial stretching in serum-free conditions. J Biomech 2004; 37: 1543-50
    CrossrefPubMedGoogle Scholar
  • 98 Almekinders LC, Baynes AJ, Bracey LW. An in vitro investigation into the effects of repetitive motion and nonsteroidal anti inflammatory medication on human tendon fibroblasts. Am J Sports Med 1995; 23: 119-23
    CrossrefPubMedGoogle Scholar
  • 99 Zeichen J, van Griensven M, Bosch U. The proliferative response of isolated human tendon fibroblasts to cyclic biaxial mechanical strain. Am J Sports Med 2000; 28: 888-92
    CrossrefPubMedGoogle Scholar
  • 100 Kannus P, Józsa KP, Renstrom P. The effects of training, immobilization and remobilization on musculoskeletal tissue, 1: Training and immobilization. Scand J Med Sci Sports 1992; 2: 100-18
    Google Scholar
  • 101 Kannus P, Jozsa L, Natri A, Jarvinen M. Effects of training, immobilization and remobilization on tendons. Scand J Med Sci Sports 1997; 7: 67-71
    PubMedGoogle Scholar
  • 102 Tanaka H, Manske PR, Pruitt DL, Larson BJ. Effect of cyclic tension on lacerated flexor tendons in vitro. J Hand Surg Am 1995; 20: 467-73
    CrossrefPubMedGoogle Scholar
  • 103 Nabeshima Y, Grood ES, Sakurai A, Herman JH. Uniaxial tension inhibits tendon collagen degradation by collagenase in vitro. J Orthop Res 1996; 14: 123-30
    CrossrefPubMedGoogle Scholar
  • 104 Buckwalter JA. Activity vs rest in the treatment of bone, soft tissue and joint injuries. Iowa Orthop J 1995; 15: 29-42
    PubMedGoogle Scholar
  • 105 Buckwalter JA. Effects of early motion on healing of musculoskeletal tissues. Hand Clin 1996; 12: 13-24
    PubMedGoogle Scholar
  • 106 Chow JA, Thomes LJ, Dovelle S, Monsivais J, Milnor WH, Jackson JP. Controlled motion rehabilitation after flexor tendon repair and grafting: A multi-centre study. J Bone Joint Surg Br 1988; 70: 591-5
    PubMedGoogle Scholar
  • 107 Cullen KW, Tolhurst P, Lang D, Page RE. Flexor tendon repair in zone 2 followed by controlled active mobilisation. J Hand Surg Br 1989; 14: 392-5
    CrossrefPubMedGoogle Scholar
  • 108 Elliot D, Moiemen NS, Flemming AF, Harris SB, Foster AJ. The rupture rate of acute flexor tendon repairs mobilized by the controlled active motion regimen. J Hand Surg Br 1994; 19: 607-12
    PubMedGoogle Scholar
  • 109 Liu Y, Ramanath HS, Wang DA. Tendon tissue engineering using scaffold enhancing strategies. Trends Biotech 2008; 26: 201-9
    CrossrefPubMedGoogle Scholar