Muscle loading is necessary for the formation of a functional tendon enthesis

Bone

Volumn 55, Issue 1, 2013, Pages 44-51

  Schwartz, A G ^a   Lipner, J H ^a   Pasteris, J D ^b   Genin, G M ^c   Thomopoulos, S ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b WASHINGTON UNIVERSITY   (United States)

^c WASHINGTON UNIVERSITY IN ST LOUIS   (United States)

Author keywords

Biomechanics; Biomineralization; Botulinum toxin A; Mechanobiology; Postnatal development; Tendon to bone insertion

Indexed keywords

BOTULINUM TOXIN A; CARBONIC ACID; COLLAGEN FIBER; HYDROXYAPATITE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIOMECHANICS; CONTROLLED STUDY; CRYSTALLOGRAPHY; FEMALE; FIBROCARTILAGE; MALE; MICROANALYSIS; MICROSCOPY; MINERALIZATION; MOUSE; MUSCLE DEVELOPMENT; MUSCLE FUNCTION; MUSCLE RIGIDITY; MUSCLE STRENGTH; MUSCULOSKELETAL SYSTEM; NONHUMAN; PARALYSIS; SHOULDER; TENDON; TENDON ENTHESIS;

ANIMALS; ANIMALS, NEWBORN; BIOMECHANICAL PHENOMENA; BONE AND BONES; BOTULINUM TOXINS, TYPE A; FIBRILLAR COLLAGENS; HUMANS; MICE; MUSCLES; PARALYSIS; TENDONS; WEIGHT-BEARING;

EID: 84876380898     PISSN: 87563282     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bone.2013.03.010     Document Type: Article

References (45)

1. Kirkos J.M., Kyrkos M.J., Kapetanos G.A., Haritidis J.H. Brachial plexus palsy secondary to birth injuries. J Bone Joint Surg Br 2005, 87:231-235.
2. Moukoko D., Ezaki M., Wilkes D., Carter P. Posterior shoulder dislocation in infants with neonatal brachial plexus palsy. J Bone Joint Surg Am 2004, 86-A:787-793.
3. Mehta S.H., Blackwell S.C., Bujold E., Sokol R.J. What factors are associated with neonatal injury following shoulder dystocia?. J Perinatol 2006, 26:85-88.
4. Hoeksma A.F., Ter Steeg A.M., Dijkstra P., Nelissen R.G., Beelen A., de Jong B.A. Shoulder contracture and osseous deformity in obstetrical brachial plexus injuries. J Bone Joint Surg Am 2003, 85-A:316-322.
5. Das R., Rich J., Kim H.M., McAlinden A., Thomopoulos S. Effects of botulinum toxin-induced paralysis on postnatal development of the supraspinatus muscle. J Orthop Res 2011, 29:281-288.
6. Thomopoulos S., Kim H.M., Rothermich S.Y., Biederstadt C., Das R., Galatz L.M. Decreased muscle loading delays maturation of the tendon enthesis during postnatal development. J Orthop Res 2007, 25:1154-1163.
7. Kim H.M., Galatz L.M., Patel N., Das R., Thomopoulos S. Recovery potential after postnatal shoulder paralysis. An animal model of neonatal brachial plexus palsy. J Bone Joint Surg Am 2009, 91:879-891.
8. Kim H.M., Galatz L.M., Das R., Patel N. Thomopoulos S. Musculoskeletal deformities secondary to neurotomy of the superior trunk of the brachial plexus in neonatal mice. J Orthop Res 2010, 28:1391-1398.
9. Schwartz A., Pasteris J., Daulton T., Genin G. Thomopoulos S. Mineral distributions at the developing tendon enthesis. PloS One 2012, 7:e48630.
10. Thomopoulos S., Marquez J.P., Weinberger B., Birman V., Genin G.M. Collagen fiber orientation at the tendon to bone insertion and its influence on stress concentrations. J Biomech 2006, 39:1842-1851.
11. Thomopoulos S., Williams G.R., Gimbel J.A., Favata M., Soslowsky L.J. Variation of biomechanical, structural, and compositional properties along the tendon to bone insertion site. J Orthop Res 2003, 21:413-419.
12. Wopenka B., Kent A., Pasteris J.D., Yoon Y., Thomopoulos S. The tendon-to-bone transition of the rotator cuff: a preliminary Raman spectroscopic study documenting the gradual mineralization across the insertion in rat tissue samples. Appl Spectrosc 2008, 62:1285-1294.
13. Genin G.M., Kent A., Birman V., Wopenka B., Pasteris J.D., Marquez P.J., et al. Functional grading of mineral and collagen in the attachment of tendon to bone. Biophys J 2009, 97:976-985.
14. Pasteris J.D., Wopenka B., Man S., Sternleib M., Yoder C. Concerning the cause of the 1070 Raman band in carbonated apatite. 8th World Biomaterials Congress 2008, Curran Associates Inc., Amsterdam.
15. Antonakos A., Liarokapis E., Leventouri T. Micro-Raman and FTIR studies of synthetic and natural apatites. Biomaterials 2007, 28:3043-3054.
16. Eliasson P., Fahlgren A., Pasternak B., Aspenberg P. Unloaded rat Achilles tendons continue to grow, but lose viscoelasticity. J Appl Physiol 2007, 103:459-463.
17. Johnson R.B., Tsao A.K., St John K.R., Betcher R.A., Tucci M.A., Benghuzzi H.A. Effects of spaceflight on the attachment of tendons to bone in the hindlimb of the pregnant rat. Anat Rec A Discov Mol Cell Evol Biol 2005, 282:147-156.
18. Sun Y.L., Thoreson A.R., Cha S.S., Zhao C., An K.N., Amadio P.C. Temporal response of canine flexor tendon to limb suspension. J Appl Physiol 2010, 109:1762-1768.
19. Foutz T., Ratterman A., Halper J. Effects of immobilization on the biomechanical properties of the broiler tibia and gastrocnemius tendon. Poult Sci 2007, 86:931-936.
20. Thomopoulos S., Fomovsky G.M., Holmes J.W. The development of structural and mechanical anisotropy in fibroblast populated collagen gels. J Biomech Eng 2005, 127:742-750.
21. Sacks M.S. Incorporation of experimentally-derived fiber orientation into a structural constitutive model for planar collagenous tissues. J Biomech Eng 2003, 125:280-287.
22. Lokshin O., Lanir Y. Micro and macro rheology of planar tissues. Biomaterials 2009, 30:3118-3127.
23. Miller K.S., Connizzo B.K., Feeney E., Soslowsky L.J. Characterizing local collagen fiber re-alignment and crimp behavior throughout mechanical testing in a mature mouse supraspinatus tendon model. J Biomech 2012, 45:2061-2065.
24. Liu Y.X., Thomopoulos S., Birman V., Li J.S., Genin G.M. Bi-material attachment through a compliant interfacial system at the tendon-to-bone insertion site. Mech Mater 2012, 44:83-92.
25. Pins G.D., Christiansen D.L., Patel R., Silver F.H. Self-assembly of collagen fibers. Influence of fibrillar alignment and decorin on mechanical properties. Biophys J 1997, 73:2164-2172.
26. Juncosa-Melvin N., Matlin K.S., Holdcraft R.W., Nirmalanandhan V.S., Butler D.L. Mechanical stimulation increases collagen type I and collagen type III gene expression of stem cell-collagen sponge constructs for patellar tendon repair. Tissue Eng 2007, 13:1219-1226.
27. Genin G.M., Birman V. Micromechanics and structural response of functionally graded, particulate-matrix, fiber-reinforced composites. Int J Solids Struct 2009, 46:2136-2150.
28. Milton G.W. The theory of composites 2002, Cambridge University Press, Cambridge.
29. Marquez J.P., Genin G.M., Zahalak G.I., Elson E.L. Thin bio-artificial tissues in plane stress: the relationship between cell and tissue strain, and an improved constitutive model. Biophys J 2005, 88:765-777.
30. Marquez J.P., Genin G.M., Zahalak G.I., Elson E.L. The relationship between cell and tissue strain in three-dimensional bio-artificial tissues. Biophys J 2005, 88:778-789.
31. Warner S.E., Sanford D.A., Becker B.A., Bain S.D., Srinivasan S., Gross T.S. Botox induced muscle paralysis rapidly degrades bone. Bone 2006, 38:257-264.
32. Poliachik S.L., Bain S.D., Threet D., Huber P., Gross T.S. Transient muscle paralysis disrupts bone homeostasis by rapid degradation of bone morphology. Bone 2010, 46:18-23.
33. Grimston S.K., Silva M.J., Civitelli R. Bone loss after temporarily induced muscle paralysis by botox is not fully recovered after 12weeks. Ann N Y Acad Sci 2007, 1116:444-460.
34. Burket J., Gourion-Arsiquaud S., Havill L.M., Baker S.P., Boskey A.L., van der Meulen M.C. Microstructure and nanomechanical properties in osteons relate to tissue and animal age. J Biomech 2011, 44:277-284.
35. Gourion-Arsiquaud S., Burket J.C., Havill L.M., DiCarlo E., Doty S.B., Mendelsohn R., et al. Spatial variation in osteonal bone properties relative to tissue and animal age. J Bone Miner Res 2009, 24:1271-1281.
36. Gamsjaeger S., Masic A., Roschger P., Kazanci M., Dunlop J.W., Klaushofer K., et al. Cortical bone composition and orientation as a function of animal and tissue age in mice by Raman spectroscopy. Bone 2010, 47:392-399.
37. Miller L.M., Little W., Schirmer A., Sheik F., Busa B., Judex S. Accretion of bone quantity and quality in the developing mouse skeleton. J Bone Miner Res 2007, 22:1037-1045.
38. Akkus O., Adar F., Schaffler M.B. Age-related changes in physicochemical properties of mineral crystals are related to impaired mechanical function of cortical bone. Bone 2004, 34:443-453.
39. Akkus O., Polyakova-Akkus A., Adar F., Schaffler M.B. Aging of microstructural compartments in human compact bone. J Bone Miner Res 2003, 18:1012-1019.
40. Aliprantis A.O., Stolina M., Kostenuik P.J., Poliachik S.L., Warner S.E., Bain S.D., et al. Transient muscle paralysis degrades bone via rapid osteoclastogenesis. FASEB J 2012, 26:1110-1118.
41. Liao S., Watari F., Xu G., Ngiam M., Ramakrishna S., Chan C.K. Morphological effects of variant carbonates in biomimetic hydroxyapatite. Mater Lett 2007, 61:3624-3628.
42. Xiao X.F., Liu R.F., Gao Y.J. Hydrothermal preparation of nanocarbonated hydroxyapatite crystallites. Mater Sci Technol 2008, 24:1199-1203.
43. Yerramshetty J.S., Akkus O. The associations between mineral crystallinity and the mechanical properties of human cortical bone. Bone 2008, 42:476-482.
44. Donnelly E., Boskey A.L., Baker S.P., van der Meulen M.C. Effects of tissue age on bone tissue material composition and nanomechanical properties in the rat cortex. J Biomed Mater Res A 2010, 92:1048-1056.
45. Anand P., Birch R. Restoration of sensory function and lack of long-term chronic pain syndromes after brachial plexus injury in human neonates. Brain 2002, 125:113-122.