Functional grading of mineral and collagen in the attachment of tendon to bone.
Attachment of dissimilar materials is a major challenge because high levels of localized stress may develop at their interfaces. An effective biologic solution to this problem exists at one of nature's most extreme interfaces: the attachment of tendon (a compliant, structural "soft tissue") to bone (a stiff, structural "hard tissue"). The goal of our study was to develop biomechanical models to describe how the tendon-to-bone insertion derives its mechanical properties. We examined the tendon-to-bone insertion and found two factors that give the tendon-to-bone transition a unique grading in mechanical properties: 1), a gradation in mineral concentration, measured by Raman spectroscopy; and 2), a gradation in collagen fiber orientation, measured by polarized light microscopy. Our measurements motivate a new physiological picture of the tissue that achieves this transition, the tendon-to-bone insertion, as a continuous, functionally graded material. Our biomechanical model suggests that the experimentally observed increase in mineral accumulation within collagen fibers can provide significant stiffening of the partially mineralized fibers, but only for concentrations of mineral above a "percolation threshold" corresponding to formation of a mechanically continuous mineral network within each collagen fiber (e.g., the case of mineral connectivity extending from one end of the fiber to the other). Increasing dispersion in the orientation distribution of collagen fibers from tendon to bone is a second major determinant of tissue stiffness. The combination of these two factors may explain the nonmonotonic variation of stiffness over the length of the tendon-to-bone insertion reported previously. Our models explain how tendon-to-bone attachment is achieved through a functionally graded material composition, and provide targets for tissue engineered surgical interventions and biomimetic material interfaces.
Genin
Guy M
GM
Department of Mechanical Aerospace and Structural Engineering, Washington University, St. Louis, Missouri 63130, USA.
Kent
Alistair
A
Birman
Victor
V
Wopenka
Brigitte
B
Pasteris
Jill D
JD
Marquez
Pablo J
PJ
Thomopoulos
Stavros
S
D000268:Adhesiveness; D000818:Animals; D001842:Bone and Bones / Q000502:physiology*; D002113:Calcification, Physiologic / Q000502:physiology*; D003094:Collagen / Q000502:physiology*; D003198:Computer Simulation; D006801:Humans; D008903:Minerals / Q000378:metabolism*; D008954:Models, Biological; D013710:Tendons / Q000502:physiology*
D008903:Minerals; D003094:Collagen
Am J Sports Med. 1999 Nov-Dec;27(6):821-30
10569374
Arch Biochem Biophys. 1996 Apr 1;328(1):135-42
8638922
J Biol Chem. 2007 Jan 12;282(2):1193-204
17052984
Proc Natl Acad Sci U S A. 2006 Jun 13;103(24):9001-5
16751282
J Biomech. 2007;40(12):2655-62
17359982
J Orthop Res. 2003 May;21(3):413-9
12706013
Appl Spectrosc. 2008 Dec;62(12):1285-94
19094386
J Biomech Eng. 2005 Jun;127(3):383-90
16060345
Ann Biomed Eng. 1999 Nov-Dec;27(6):712-20
10625144
J Struct Biol. 2007 Feb;157(2):365-70
17055741
Matrix Biol. 1998 Apr;17(1):65-73
9628253
Biophys J. 2005 Feb;88(2):778-89
15596491
J Biomech Eng. 1985 May;107(2):158-65
3999712
J Biomech. 2006;39(10):1842-51
16024026
Biomech Model Mechanobiol. 2008 Feb;7(1):13-26
17297632
Proc Natl Acad Sci U S A. 2006 Nov 14;103(46):17249-54
17088555
J Hand Surg Am. 1977 Jan;2(1):66-9
839056
Matrix Biol. 1998 Mar;16(8):457-70
9550263
J Struct Biol. 1999 Jun 30;126(3):241-55
10475685
J Shoulder Elbow Surg. 1996 Sep-Oct;5(5):383-92
8933461
J Biomech. 2004 Apr;37(4):549-56
14996567
Proc Natl Acad Sci U S A. 2006 Nov 21;103(47):17741-6
17095608
Biochem J. 1996 Jul 1;317 ( Pt 1):59-64
8694787
J Bone Joint Surg Am. 2004 Feb;86(2):219-24
14960664
J Physiol. 1999 Nov 15;521 Pt 1:307-13
10562354
J Bone Joint Surg Am. 1991 Aug;73(7):982-9
1874784
Biophys J. 2008 Mar 15;94(6):2204-11
18032556
J Orthop Res. 2004 May;22(3):607-12
15099642
Nat Mater. 2007 Jun;6(6):454-62
17515917
Biophys J. 2008 Mar 15;94(6):2361-73
18065452
J Biomech Eng. 2003 Oct;125(5):726-31
14618932
Comp Biochem Physiol A Mol Integr Physiol. 2002 Dec;133(4):931-45
12485684
J Biomech Eng. 2003 Feb;125(1):106-13
12661203