Journal Club Theme of June 2009: Bimaterial interfaces in nature: attachment of tendon to bone

The June journal club entry was written jointly with Stavros Thomopoulos  from the Department of Orthopaedic Surgery at the Washington University in St. Louis School of Medicine.

Attachment of dissimilar materials is a materials engineering challenge because of high levels of localized stress that can arise at a bimaterial interface.  While stress concentrations can arise outside of an inclusion, the problem is of particular interest when the bimaterial interface has an exposed edge: in some instances, an elastic singularity can arise at the interface (e.g.,Williams, ML. 1952. "Stress singularities resulting from various boundary conditions in angular corners of plates in extension." Journal of Applied Mechanics19: 526-528.)  When one of the materials can form a fracture process zone, an interface can be designed so that even a cracked interface can withstand a design load (e.g. Hutchinson, J.W., Suo, Z., "MixedMode Cracking in Layered Materials." Advances in Applied Mechanics edited by J. W. Hutchinson and T. Y. Wu, 29, 63-191 (1992).)  The idea here is that, in such a case, the singularity is masked by a fracture process zone in which material simultaneously absorbs energy and shields the crack tip from the highest stresses through a reduction in stiffness.  A host of “functional grading” schemes exist in which the material properties of neighboring materials are interpolated over an interfacial zone; these can further toughen the interfaces (see, for example, the set of papers in Eng. Fract. Mech. 69(14-16), 2002; a recent review is Birman V and Byrd LW “Modeling and Analysis of Functionally Graded Materials and Structures” Appl. Mech. Rev. 60, 2007 ). 

But all this is simple compared to the problem of attaching two biological tissues.  Biological tissues often stiffen with stretched instead of strain hardening, meaning that stress concentrations become amplified with increased stretch, rather than shielded as in the case of metals.  How does nature handle the problem?  We are particularly interested in the way the body attaches tendon to bone: this is nature’s greatest material mismatch for a tensile structural connection, about the same mismatch as that between a ripe grape and its stem.

How does the body achieve this attachment?  In addition to providing the tendon with an outward splay, the body presents a functional grading scheme that differs from any we have observed in engineering practice.  Rather than interpolating between tendon and bone, as an engineer might do, the body incorporates a band of tissue that is more compliant than either tendon or bone (Thomopoulos, S., G. R. Williams, J. A.Gimbel, M. Favata, and L. J. Soslowsky. 2003. Variation of biomechanical, structural,and compositional properties along the tendon to bone insertion site.Journal ofOrthopaedic Research 21:413-419).  A joint paper coming out from our group this summer shows that this arises from a reduction in collagen organization and an increase in mineralization between tendon and bone; the drop in stiffness ends after the percolation threshold in mineralization is reached.

We are interested in how the body achieves this not only to inform biomimetic bimaterial interface design, but also for design of engineered surgical grafts.  Our surgical colleagues need these desperately: in reattachment of rotator cuff tendons to the humeral head of the shoulder, the standard reattachment procedure involves snipping off all of the (usually frayed) transitional tissue and sewing the tendon straight onto the bone. Recurrance of tears with this approachis as high as 94% in some populations (Don’t believe us?  See Galatz, L. M., C. M. Ball, S. A. Teefey,W. D. Middleton, and K. Yamaguchi. 2004. "The outcome and repair integrity of completelyarthroscopically repaired large and massive rotator cuff tears," Journal of Bone& Joint Surgery - American Volume 86-A:219-224.)  To this end we are building surgical grafts for tissue-to-bone attachments in tension (e.g., see Kappa Delta award paper from Stavros Thomopoulos: http://www.aaos.org/Research/committee/research/Kappa/kappa_winners.asp#2009 ),and others are building grafts for compressive links, (e.g., Harley BA, Lynn AK,Wissner-Gross Z, Bonfield W, Yannas IV, Gibson LJ. "Design of a multiphase osteochondral scaffold. II. Fabrication of a mineralized collagen-glycosaminoglycan scaffold," J Biomed Mater Res A, 2009, PMID: 19301274).

We have a good sense of “how,” but we would like to begin the discussion of “why?”  Why include a compliant band in the middle of what is already nature’s most severe material mismatch?  Another article from our group to appear this summer indicates that, in some instances, stress concentrations can be reduced by a functional grading of the unusual character observed in nature.  But we suspect the answer is deeper, and that nanoscale simulations might shed light on the question.  Wewould like to open the floor for discussion by highlighting two contributions from the group of Markus Buehler:

The first is Buehler, M.J., and Ackbarow, T., “Nanomechanical strength mechanism of hierarchical biologicalmaterials and tissues,” Computer Methods in Biomechanics and Biomedical Engineering, 2008 .  Here, the authors predict the remarkable result that collagen fibrils are tougher at higher strain rates.  Could it be that the collagen in the compliant band between tendonand bone is actually tougher because of partial mineralization that increases strainrates between pockets of mineralization?

The second is Buehler, M.J., “Molecular nanomechanics of nascent bone: fibrillar toughening by mineralization,” Nanotechnology, 2008 .  Here, Markus shows that, if one allows for slippage at the interface between collagen and mineral, a mineralized collagen fibrilis much tougher than an un-mineralized one. Could it be that, in regions of partial mineralization, enhanced mineral mobility leads to increased toughness?

We hope that you will have some ideas on the subject.  Note that we like Markus and recognize that he had to make some assumptions in these studies, so please go easy on this aspect of the work unless you happen to be an experimentalist with an idea of how to prove any of these assumptions wrong.